Neuroscience and Biobehavioral Reviews 128 (2021) 592–620

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Neuroscience and Biobehavioral Reviews

journal homepage: www.elsevier.com/locate/neubiorev

Review article

The neuroscience of social feelings: mechanisms of adaptive

social functioning
Paul J. Eslinger a, *, Silke Anders b, Tommaso Ballarini c, Sydney Boutros d, Sören Krach e,
Annalina V. Mayer e, Jorge Moll f, Tamara L. Newton g, Matthias L. Schroeter h,
Ricardo de Oliveira-Souza i, Jacob Raber j, Gavin B. Sullivan k, James E. Swain l, Leroy Lowe m,
Roland Zahn n
a
Departments of Neurology, Neural & Behavioral Sciences, Pediatrics, and Radiology, Penn State Hershey Medical Center, Hershey, PA, USA
b
Social and Affective Neuroscience, Department of Neurology, University of Lübeck, Lübeck, Germany
c
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
d
Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, USA
e
Social Neuroscience Lab, Translational Psychiatry Unit, University of Lübeck, Lübeck, Germany
f
Cognitive Neuroscience Unit, D’Or Institute for Research and Education (IDOR), Rio de Janeiro, Brazil
g
University of Louisville, Department of Psychological and Brain Sciences, Louisville, KY, USA
h
Max Planck Institute for Human Cognitive and Brain Sciences, Clinic for Cognitive Neurology, University Hospital Leipzig, Leipzig, Germany
i
Cognitive Neuroscience Unit, D’Or Institute for Research and Education (IDOR), BR Hospital Universitario, Universidade do Rio de Janeiro, Brazil
j
Departments of Behavioral Neuroscience, Neurology, and Radiation Medicine, Division of Neuroscience, ONPRC, Oregon Health & Science University, Portland, OR,
USA
k
International Psychoanalytic University, Berlin, Germany, Centre for Trust, Peace and Social Relations, Coventry University, UK
l
Department of Psychiatry and Behavioral Health, Psychology and Obstetrics and Gynecology, Renaissance School of Medicine at Stony Brook University, Stony Brook,
NY, USA
m
Neuroqualia (NGO), Truro, NS, Canada
n
Centre for Affective Disorders, Institute of Psychiatry, Psychology & Neuroscience, King’s College London, UK

A R T I C L E I N F O A B S T R A C T

Keywords: Social feelings have conceptual and empirical connections with affect and emotion. In this review, we discuss
Social feelings how they relate to cognition, emotion, behavior and well-being. We examine the functional neuroanatomy and
Empathy neurobiology of social feelings and their role in adaptive social functioning. Existing neuroscience literature is
Second person neuroscience
reviewed to identify concepts, methods and challenges that might be addressed by social feelings research.
Social affiliation
Social influence
Specific topic areas highlight the influence and modulation of social feelings on interpersonal affiliation, parent-
Social media child attachments, moral sentiments, interpersonal stressors, and emotional communication. Brain regions
Parent-child attachment involved in social feelings were confirmed by meta-analysis using the Neurosynth platform for large-scale,
Moral sentiments automated synthesis of functional magnetic resonance imaging data. Words that relate specifically to social
Interpersonal stressors feelings were identfied as potential research variables. Topical inquiries into social media behaviors, loneliness,
Emotional communication trauma, and social sensitivity, especially with recent physical distancing for guarding public and personal health,
Loneliness underscored the increasing importance of social feelings for affective and second person neuroscience research
Trauma
with implications for brain development, physical and mental health, and lifelong adaptive functioning.

1. Introduction aspects of survival and life regulation (Buck, 1985; Damasio and Car­
valho, 2013; LeDoux, 2012; Panksepp, 2010; Strigo and Craig, 2016).
A "feeling" is a fundamental construct in the behavioral, neurobio­ Feelings may sometimes signify a sensation, an emotion, perception, a
logical and social psychological sciences encompassing a range of sub­ form of thought (e.g., judgement, sense), impression or opinion, an
jective experiences. Many of these experiences relate to homeostatic inclination to believe, or an overall physical (e.g., feeling ill) or

* Corresponding author at: Department of Neurology, Penn State Hershey Medical Center, 30 Hope Drive EC037, PO Box 859, Hershey, PA, 17033-0859, USA.
E-mail address: peslinger@pennstatehealth.psu.edu (P.J. Eslinger).

https://doi.org/10.1016/j.neubiorev.2021.05.028
Received 3 August 2020; Received in revised form 31 January 2021; Accepted 10 May 2021
Available online 2 June 2021
0149-7634/© 2021 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
P.J. Eslinger et al. Neuroscience and Biobehavioral Reviews 128 (2021) 592–620

psychological experience (e.g., feeling excluded). It is important to summarizing future research needs in this burgeoning domain.1
distinguish that feelings as affections “are categorically distinct from
cognition and from feelings that are sensations which, unlike affections, 2. The concept of social feelings
have a bodily location and may inform one about the state of one’s
body” (Bennett and Hacker, 2003) (p. 199). Damasio and Carvalho Social feelings occupy an important position in relationship to
(2013) argued that the bodily “viscera” are critical to many feelings or empiricial research and affect and emotion theory, particularly
are distinct from specific emotions. Although feelings are fundamentally involving interpersonal contexts. Their presence and potential influence
private, inner experiences, they nevertheless may be inferred from or can vary from fleeting to long-term feeling states intertwined with
perceived directly in the public behavior of people (e.g., behavioral complex chains of thoughts, emotions and behaviors. Temporal aspects
criteria can be used to teach another person about complex social feel­ of social feelings are not yet well understood. They can reflect psycho­
ings; Bennett and Hacker, 2003). logical and viscero-somatic comfort and security as well as discomfort
A broad definition for feeling is a subjective experience that appears that has social origins (e.g., “cringing” at the remarks of another person
to emerge from perceptions and mental events involving processes in­ (Müller-Pinzler et al., 2016). Social feelings may indicate one’s current
side and outside the central nervous system as well as physiological/ standing in relation to others, highlight the importance of the thoughts
bodily states (Damasio and Carvalho, 2013; LeDoux, 2012; Nummen­ and feelings of other individuals and groups, have specific normatively
maa et al., 2016) in interpersonal and other environmental contexts. and culturally constructed expressive forms, and contribute to a wide
However, the full range of feelings is diverse. It has been posited that variety of effects and functions (Dan Glauser and Scherer, 2008). For
they can emerge from and with emotions (Buck, 1985; Damasio and example, a sincere apology because of a social faux pas can, once
Carvalho, 2013; Panksepp, 2010), levels of arousal, physical actions and accepted by the person or group harmed, reduce feelings of regret and
activities (Bernroider and Panksepp, 2011; Gardiner, 2015; Kirsch et al., guilt about one’s initial actions concerning another. It is also possible to
2018), linguistic and social acts (Lindquist et al., 2012), hedonics be influenced by the emotions experienced by others not simply because
(pleasure and pain) (Buck, 1985; Damasio and Carvalho, 2013; LeDoux, they are other people but especially because they are members of one’s
2012; Panksepp, 2010), drives (Alcaro and Panksepp, 2011; Damasio own social group. The currency of shared and unexpressed feelings ap­
and Carvalho, 2013), cognitions including perceptions/appraisals of self pears to potentially fuel, discourage as well as segregate many kinds of
and others (Ellemers, 2012; Frewen et al., 2013; Northoff et al., 2009), social actions and relationships. Yet, feelings are often not clearly
motives (Higgins and Pittman, 2008), social interactions (Damasio and considered or accounted for in many social neuroscience models
Carvalho, 2013; LeDoux, 2012; Panksepp, 2010) as well as reflective although they are acknowledged as key component processes (e.g.,
(Holland and Kensinger, 2010), emerging (e.g., the importance of Bickart et al., 2014; Porcelli et al., 2019).
oscillatory activity to consciousness of the feeling component of emotion Advances in affective research have revealed important distinctions
(Dan Glauser and Scherer, 2008)) and anticipatory perspectives (Buck, between feelings and emotions. Feelings are considered an affective
1985; Miloyan and Suddendorf, 2015). Embodied and enacted experi­ component/constituent of emotional responses. For example, fear as an
ences and activities create meaning through the visceral, haptic, kines­ emotion consists of a spectrum of automatically activated cognitive re­
thetic and sensual systems that may well feed into feelings caused by or actions and defense behaviors that co-occur along with “feelings of fear”
manifested in social situations. While Schilbach et al. (2013) and others that can encompass changes in hormonal, viscero-somatic and mental
have delineated how experiencing and interacting with others can be state processing. Emotions are distinguished from feelings in that they
primary ways of knowing others, feelings likely play important roles in tend to be more complex, parcellated, cognitively elaborated and
these social processes and may provide underlying mechanisms that semantically filtered. It is also important to note that feelings are not
influence and modulate behavior. limited to those that co-occur with specific emotions. Rather, feelings
In this review, we consider social feelings, which we more narrowly encompass a wide range of important mental experiences that may
describe as subjective experiences that arise in interaction with others or signify physiological need (e.g., hunger), tissue injury (e.g., pain),
when being remembered and when recalling others’ behaviors, valenced features of behavior that are not always “felt” (Winkielman
thoughts, intentions or emotions. Specifically, we reviewed neurosci­ and Berridge, 2004), optimal function (e.g., well-being), discord, and
ence research on social feelings that has been conducted. We considered dynamics of social synchrony such as increases or decreases in social
whether the notion of ‘social feelings’ represented natural kinds of status. We observed that feelings are not consistently defined in the
neurobiological processes that could be identifiable and conducive to social neuroscience literature, and that definitions for these terms can
scientific inquiry. That is, alongside emotion, attitudes and the self, evolve with new discoveries. Moreover, while the natural occurrence of
feelings appear to be naturally occurring phenomena and especially some social feelings may be universally experienced across cultures (e.g.,
prominent within social contexts (Mitchell, 2009). As part of this review, grief, affiliation, parental love etc.), we acknowledge that aspects of
we (1) discussed the fundamental importance of social feelings for other social feelings may be culturally shaped. Their roles as influencers
attachment, affiliation, empathy, influence and well-being, dis­ and modulators will be examined in several developing research lines.
tinguishing it from emotions; (2) considered its emerging role in Within psychology and the neurosciences, there is a growing
research areas of parent-child attachments, moral sentiments, interper­ awareness that feelings are an important but neglected topic that is
sonal stress, and emotional communications, while acknowledging
important neurotransmitter and neurohormonal modulators; (3)
confirmed by meta-analysis the brain regions involved in social feelings,
using the Neurosynth platform for large-scale, automated synthesis of 1
This review of ‘social feelings’ was undertaken as part of the ‘The Human
functional magnetic resonance imaging (fMRI) data; (4) explored the Affectome Project’, an initiative organized in 2016 by the non-profit organi­
rising importance of social feelings research in psychiatric disorders and zation Neuroqualia (https://www.neuroqualia.org). As part of the Human
in the era of expanding social media during periods when physical Affectome project, a series of overarching reviews is being published that
distancing has been required for guarding public and personal health; summarize and critique much of what is currently known about affective
neuroscience while simultaneously exploring the language that we use to
(5) reviewed the language that people use to express social feelings and
convey feelings and emotions. The project is comprised of twelve teams that are
whether those terms might inform the way we approach social neuro­
organized into a taskforce focused on the development of a comprehensive and
science research (Fig. 1); and (6) identified the relationships that exist integrated model of affect that could serve as a common focal point for current
between social feelings and other areas of affective research within this and future affective research. Recent papers of this effort pertinent to social
special issue (i.e., Physiological, the Self, Anticipatory, Actions, Atten­ feelings include those on fear (Raber et al., 2019), self (Frewen et al., 2020) and
tion, Motivation, Anger, Fear, Happiness, Sadness, and Hedonics), anticipatory feelings (Stefanova et al., 2020).

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Fig. 1. Overview of the contents of the review.

We discuss social feelings in the context of 5
major sub-categories: Affiliation, Parent-Child
Attachment, Moral Sentiments, Interpersonal
Stressors, and Emotional Communication.
Throughout, we consider the known neurobi­
ology related to social feelings and highlight
where research is needed. Additionally, we re­
view the language people use to express social
feelings, and included a meta-analysis using
Neurosynth software. This review is timely,
considering the growth in social media and
recent world-wide interest in the psychology of
social interaction and social distancing, with
their effects on overall well-being.

distinct from the topic of emotion. Similar to the many covert and overt perceiving and evaluating the actions of others as well as deciding how
dimensions of emotion (Cowen and Keltner, 2017), there is recognition to respond within social interactions (Gilam and Hendler, 2016). As
that feelings also may serve overt as well as covert purposes. It has been important conceptual and methodological challenges, we first address
hypothesized that feelings may guide caution or confirm cognitions in emotional contagion, empathy, attachment and affiliation as mediating
social and non-social settings (e.g., something doesn’t feel right here, processes.
this person makes me feel uneasy). Recent ideas from the ‘second person
neuroscience’ literature (e.g., Pfeiffer et al., 2013) have emphasized that 2.1. Social feelings: contagion, empathy, attachment and affiliation
interpersonal contexts can invoke social network processes, some of
which may be experienced as involuntary (e.g., mirror neuron system Social feelings appear to be generated through a variety of mediating
and emotional contagion) and others as inferential, derived from prior processes. Their effects can be fleeting or persistently impact mental
experiences or mentalizing network activity associated with a multi­ experiences and behavior. Prominent explanations to date for genera­
plicity of social feelings. We are interested in addressing how the tion of social feelings in relation to persons and groups have included
construct of social feelings relates to social cognition and social emo­ contagion and empathy. The intentional communication and sharing of
tions. For example, reactive feelings to another in the case of some in­ feelings involving others can lead to various forms of influence upon one
stances of stigma and disgust can be reduced by a shared social identity another. Research on emotional contagion has revealed that experiences
(Reicher et al., 2016), possibly indicating the greater importance of of emotional empathy, for example, facilitates “somatic, sensory, and
inhibitory processes as correlated lateral prefrontal cortex (PFC) and motor representations of other people’s mental states” (Nummenmaa
anterior cingulate cortical (ACC) responses increase (Krendl et al., et al., 2008) (p. 571). Explanations have focused on the proposed mirror
2006). Contagion remains an elusive and problematic concept (e.g., neuron system and the automatic activation of motor and sensory sys­
when understood as a kind of virus-like transmission between people tem representations of observed behaviors of others with linkage to
and within groups), as the strength of involuntary sharing of feelings and limbic system structures as a potential basis for some of the shared
emotional states with others can be influenced by age, context, and feelings of empathy (Carr et al., 2003; Nummenmaa et al., 2008; Keysers
group dynamics. For this reason concepts such as influence and ampli­ and Gazzola, 2009). Similar research in social contagion has examined
fication of feelings are important to consider as there are implications some of the physiological correlates of synchronized feelings and shared
for understanding how feelings may trigger a variety of mechanisms (e. social emotions that can occur in typical group settings (Ardizzi et al.,
g., approach, avoid, imagined social status) through which people affect 2020). While the neurophysiological bases of social feelings often arises
and are affected by others. We suspect that these dynamics can be some in interaction with individuals, it is also important to explore instances
of the key roles of feelings in social action and interaction. of social influence in groups. This can include sharing feelings with a
Social feelings appear to relate to well-being pertinent to maintain­ group and the experience of having one’s feelings “amplified” by others
ing homeostasis. Social behaviors and interactions can be particularly when acting towards joint aims or goals (e.g., feeling empowered (Drury
susceptible to influence and modulation by feelings. This obtains for et al., 2005) or collective pride (Sullivan, 2017)).

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Research on the neural systems responsible for processes of social inaccurately as the possible start of a relationship). Social interactions
contagion has been limited by experimental situations and tasks, but is where there is a discrepancy between one’s own feelings and those of
still developing. When healthy participants viewed emotionally-charged another person pose an interesting research challenge as well. Neural
social scenes and were instructed to empathize with a specific person in systems involving the pregenual anterior cingulate cortex (pACC) may
the scene (i.e., emotional empathy), for example, significant activations have a role in generating unpleasant feelings and have been associated
in the parietal (secondary somatosensory and inferior regions), fusiform, with feelings of suffering (Vogt, 2005) such as when the presence or
middle frontal and parahippocampal cortices as well as insula, thalamus actions of another person are deeply distressing. Therefore, social feel­
and brainstem were detected than when instructed to empathize with a ings potentially have multiple ways of influencing and modulating ac­
person in a non-emotional social scene (i.e., cognitive empathy) tions that have individual or multi-person significance.
(Nummenmaa et al., 2008) (Fig. 2A). These systems might be involved Among social feelings, so-called ‘affiliative feelings’ are purported to
in the experience of what the other person is feeling. Automatic and play a central role in interpersonal relations (e.g., parental, romantic,
rapid generation of similar feelings may lead to further sharing, mimicry friendship, organizational), as they embed key building blocks for
(expressive or communicative), matching of emotional behavior (e.g., human attachment and bonding. These may be germane to the potential
smiling, celebrating), and coordination of social activities (e.g., group for effective adaptation and more complex social feelings such as guilt,
singing, coordinated actions). compassion and gratitude. Affiliative feelings, moreover, may be a
A natural extension of influence, empathy and emotional contagion fundamental driving force undergirding socially motivated behavior
into the social domain pertains to the neuroscience of feelings of that is associated with natural rewards (e.g., pride in the laudable be­
belongingness produced by bonding and identification at the group- haviors of others one is closely related to) (Warnell et al., 2018).
level. These investigations have provided evidence of other brain re­ Feelings also have been tightly linked to a wide spectrum of activities
gions associated with what can be described as ‘like love’ (Duarte et al., described as socio-moral. Feelings are said to be moral when they
2017) and may involve experiences of group-based pride. We would involve the interests or welfare either of society as a whole or at least of
expect that the latter might activate similar regions as individual pride persons other than the judge or agent (Haidt, 2003). Because these
and include the right posterior superior temporal sulcus and left tem­ feelings may help aggregate, civilly space or alienate humans, they are
poral pole (Takahashi et al., 2008) (Fig. 2B). An fMRI study of football often categorized into a spectrum of prosocial and anti-social classes
fans watching videos of their team vs. a rival team reported higher levels (Fontenelle et al., 2015; Thoits, 1989). Prosocial feelings are feelings
of activation in a network involving the ventral tegmental area, sub­ related to positive interactions with others (e.g., cooperation, helping,
stantia nigra, striatum, insula, hippocampus and amygdala (Duarte reciprocity, reparative actions). Similarly, prosocial feelings are also
et al., 2017) (Fig. 2C). The results support an interpretation of activation related to social conformity and involve feelings such as guilt, embar­
of reward and affective processing systems. Similarly, such results rassment, gratitude and awe (Moll et al., 2008b) (Fig. 3). Prosocial
demonstrate the difficulty of attempting to easily localize neural systems feelings include varying degrees of affiliative feelings, which are key for
mediating feelings that are not intense enough, enduring or are not yet social attachments, whether parent-infant, filial, friend, neighbor or
imbricated with reasons, goals and evaluations to be described in terms other.
of emotions but often may still be of considerable psychological and Attachment to nonhuman living beings (e.g., plants, homes, personal
social importance (Cikara and Van Bavel, 2014). effects), cultural symbols, abstract ideas, and beliefs (the so-called
Although recent theoretical efforts have given feelings a central role “extended attachment”) may contribute to the remarkable human
in psychology (Cromby, 2015; Damasio and Carvalho, 2013), there re­ inclination to cooperate beyond kinship boundaries, due to intrinsic
mains a gap in understanding what contributes to a person’s feelings reward, even when no evident reputation gains are at stake (Moll and de
being markedly different to many others. Cromby’s analysis of the Oliveira-Souza, 2009). As such, affiliative feeling may be proposed a
neurophysiological underpinnings of feelings of paranoia—that others cornerstone for several prosocial emotions (i.e. guilt, gratitude and
are a potential or immediate threat—may be a useful example to compassion) (Moll and Schulkin, 2009; Moll et al., 2011; Preston, 2013),
consider here before exploring specific empirical studies (e.g., see Sec­ but not for those that drive social conformity based on self-interested
tion 9 for examples of research social feelings and psychiatric condi­ motivation (e.g., embarrassment) (James and Olson, 2000). In
tions). Describing the resultant feelings as “unfounded fears” (Freeman contrast, sentiments linked to interpersonal aversion – the other-critical
et al., 2015) does not quite capture the diverse qualitative feelings sentiments (such as disgust, contempt and anger/indignation) – are
associated with the experience of paranoia that include threat, disap­ experienced when others violate norms or one’s rights or expectations,
proval, humiliation and powerlessness. For this reason, Cromby and and endorse aggression, punishment, group dissolution and social
Harper (2009) conclude “there is no account either of the variety of reorganization (Haidt, 2003; Moll et al., 2005) (Fig. 3). In the latter
feelings related to paranoia, or of the ways in which they may be study, neural activations evoked by social disgust, interestingly, over­
related” (p. 341). Freeman et al.’s approach emphasized multiple causal lapped to a large extent with those evoked by sensory (e.g., putrid taste
roles for paranoid delusional feelings (e.g., on-going stress, illicit drugs, or odor) disgust. Hence, a more reflexive, self-protective action may
and trauma). With regard to the links between suspected neural systems power a similar type of socially aversive feeling. Hence, acquired norms
and such feelings, there have been only a few attempts in psychological of social behavior may set parameters within which affects spur
research to associate these particular neural systems or any other breaking off contact or affiliating with agents and/or their actions, as
embodied aspects of emotion with cognitive accounts of paranoia well as other approach-avoidance tendencies.
(Damasio, 1994) (p. 342). It is particularly important here that Comby A key question that remained unsolved until recently was whether
and Harper highlight “impoverished notions of social influence” (p. 342) brain activation associated with affiliative feelings could be anatomi­
as a key problem for a convincing account of the affects accompanying cally and functionally dissociated from general positive or negative
paranoia. emotional states. One recent study employed passive presentation of
It is interesting to consider that we are not always aware of the social narratives involving kin (i.e., associated with affiliative states) or
processes that give rise to feelings. For example, irritability might be a not involving kinship (Moll et al., 2012) and confirmed the prediction
measured response to the unreasonable actions of others, or it might be that the septo-hypothalamic region would be engaged by affiliative
due to low blood sugar, tiredness or other non-social concern. Cromby states in both positive and negative emotional scenarios. Interestingly,
and Harper (2009) also noted that we may not be aware of what activity in another basal forebrain region, the subgenual cingulate cor­
prompted a particular feeling or our interpretation of it may be incor­ tex, was only detected when modelling individual differences in how
rect. This might be particularly true of social feelings (e.g., the thrill of strongly participants perceived their own families as a distinctive social
being accidentally touched by someone might be interpreted group in affiliative scenarios (Rusch et al., 2014). These results

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Fig. 2. Brain regions associated with empathy. A) People

instructed to look at interpersonal scenes and empathize
with a specific person in an emotionally-charged vs.
neutral situation showed greater activation in premotor
cortex, thalamus, primary motor cortex, and primary
somatosensory cortex. Participants simultaneously re­
ported feeling similar emotions to the "other” person
(Nummenmaa et al., 2008). B) Evidence for “group”
emotions point to activation of the right posterior supe­
rior temporal sulcus and the left temporal pole, regions
that are similarly activated when individuals feel pride in
themselves (Takahashi et al., 2008). C) Other in­
vestigations into “group” feelings have shown that the
striatum, substantia nigra, ventral tegmental area, insula,
hippocampus, and amygdala have an increase in activa­
tion when sports fans watch emotionally-charged clips of
their favorite teams (Duarte et al., 2017).

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physical space but also according to social relational frames such as

power, dominance hierarchy, familiarity, kinship, and other socially
relevant processes that organize one’s social networks within different
settings and contexts. This can lead to new testable hypotheses utilizing
computation approaches to increase understanding of social
decision-making (Charpentier and O’Doherty, 2018). We anticipate that
such studies will reveal affiliative feelings as being contributing factors.

3. Arginine, vasopressin, and oxytocin within the social

behavior neural network

The neural network that mediates and influences social behavior has
been referred to as the social behavior neural network (SBNN) (New­
man, 1999) (Figs. 4 and 5). This large scale cortical-subcortical network
includes frontomedial prefrontal cortex (PFC), cortex of the tempor­
oparietal junction (TPJ), precuneus, amygdala and other structures or
nodes that are strongly regulated by hormonal effects and are conserved
across mammalian species. Of particular interest for this discussion are
the nodes including the posterior bed nucleus of the stria terminalis
(BNSTp), lateral septum (LS), medial preoptic area (MPOA), ventro­
medial hypothalamus (VMH), anterior hypothalamus (AH), and peri­
aqueductal grey (PAG) (Fig. 4). Common characteristics of these nodes
are that they all (1) contain gonadal hormone receptors, (2) are recip­
rocally interconnected, and (3) they have been recognized for their
regulatory contributions to social behavior (including aggression, sexual
behavior, social recognition memory, parental behavior and social
Fig. 3. Schematic illustration of one of the ways social feelings can be broken communication (Adkins-Regan, 2009; Albers, 2012, 2015; Albers et al.,
down. Feelings of affiliation greatly depend on the individual’s perception of 2002; Bosch and Neumann, 2012; Goodson and Kingsbury, 2013). This
the other’s feelings. Generally, these can be grouped as having a negative or network appears to be evolutionarily conserved and exists in mamma­
positive valence, and being self- or other-oriented. Additionally, morality is a
lian species and in non-mammalian vertebrates (Crews, 2003; Goodson,
large component of shared feelings, which can be grouped widely into pro-
2005; O’Connell and Hofmann, 2011), although important differences
social or social-aversive. Examples of pro-social affiliative emotions include
may exist in non-mammalian networks (Goodson and Kingsbury, 2013).
compassion, guilt, embarrassment, gratitude, and awe, and serve to build &
foster relationships. Examples of social-aversive affiliative emotions include The working hypothesis for researchers in this field is that social
disgust, contempt, anger, and indignation, which often lead to social aversion behavior across a wide range of species is influenced by interactions
or a break-down of potential relationships. within the nodes of this network (Albers, 2015).
Within this network, there is a substantial evidence that arginine-
suggested a more sophisticated role for the subgenual cingulate cortex in vasotocin (AVT)/arginine vasopressin (AVP) and oxytocin (OT) neuro­
encoding social group belongingness. Bortolini et al. (Bortolini et al., peptides have a significant influence on social behavior (Albers, 2015).
2017) confirmed the role of subgenual frontal areas in distinguishing In humans, polymorphisms in the genes encoding oxytocin and vaso­
between in- and outgroups by showing that the subgenual cortex was pressin peptides and/or their respective target receptors have been
selectively activated for efforts benefitting anonymous fellow fans of associated with variation in social recognition (Tobin et al., 2010), so­
one’s soccer club compared with playing to benefit non-fans. cial attachment (Tickerhoof and Smith, 2017), parental behavior
Activation of basal forebrain regions was also observed in fMRI ex­ (Johnson and Young, 2017), affective disorders (Surget and Belzung,
periments involving healthy participants witnessing the delivery of re­ 2008) and psychiatric phenotypes such as autism (Cataldo et al., 2018)
wards to similar others (“vicarious rewards” (Anders et al., 2020a; There are two main classifications of vasopressin receptors (i.e.,
Mobbs et al., 2009)). In this study, watching another player with whom Avpr1 and Avpr2). Subtype Avpr1a is a transmembrane G-protein-
one could identify receiving rewards was associated with activation of coupled receptor found in several brain nuclei and is involved in the
the ventral striatum and adjoining septo-hypothalamic area. Interest­ regulation a range of social behaviors, including sibling conflict,
ingly, when correlated with the perceived degree of similarity of shared agreeableness and impulsive aggression (Mulholland et al., 2020;
values (a more complex construct), higher activity was observed in the Phelps, 2010; Wilson et al., 2017). Avpr1b, by contrast, is quite localized
subgenual frontal cortex. within the brain (prominent in hippocampal CA2 pyramidal cells and in
Affiliative feelings, therefore, comprise subjective experiences asso­ anterior pituitary corticotrophs) and is an important modulator of stress
ciated with fundamental social behaviors (such as when parents hold adaptation via the hypothalamic-pituitary-adrenal (HPA) axis (Caldwell
offspring in their arms) as well as more elaborated ones in diverse social et al., 2017; Roper et al., 2011), as well as aggressive behavior, and
contexts associated with emotional overtones and sophisticated cogni­ social memory (Stevenson and Caldwell, 2012).
tive processing. The circuitry of the human brain that enables affiliative The OT receptor (Oxtr) is a transmembrane G-protein-coupled re­
feelings has so far pointed to the importance of the hypothalamic, septal, ceptor and the primary mechanism for oxytocin effects within the cen­
striatal and subgenual frontal areas of the brain together with hormonal tral nervous system (Caldwell, 2017). Brain regions dense in OT and OT
modulation influences and network interactions with other limbic sys­ receptors (among other neuropeptides and monoamines) include the
tem and cortical networks related to social behaviors. pre-optic anterior hypothalamic area, the septal region and closely
An emerging framework for considering diverse forms of affiliation associated basal forebrain structures. OT and its receptors have been
has proposed that the hippocampus and related structures map rela­ primarily associated with positive social behaviors, such as social
tional aspects of affiliation to help organize such information for reward learning (Dolen et al., 2013), regulating maternal behaviors
behavioral actions (Montagrin et al., 2018; Schafer and Schiller, 2018). (Marlin et al., 2015), social learning of trust (Xu et al., 2019) and social
Mapping computations may organize conspecifics not only according to attachment (Carter, 2017) (see (Jurek and Neumann, 2018) for a full
review). However, there is an increasing understanding that it also

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Fig. 4. The social behavior neural network (Adapted from Smith et al., 2019a,b): Green boxes represent cortico-striatal regions; red box represents midbrain region;
blue boxes represent hypothalamic regions.

Fig. 5. Importance of oxytocin in pair bonding

and maternal feelings. Oxytocin (OT) has been
identified as an essential neurochemical in the
formation of social attachment. Brain regions
dense in OT and OT receptors (among other
neuropeptides and monoamines) include the
pre-optic anterior hypothalamic area, the septal
region, and closely associated basal forebrain
structures. Damage to this system interrupts
naturally occurring monogamous pair-bonds in
prairie voles, and formation of mother-child
attachments.

mediates an important role in the avoidance of social contexts (Steinman genetically-modified animals associated with reduced receptors for
et al., 2019), leading some to suggest that it plays a critical role in oxytocin (OT) in that region reported disrupted maternal caregiving
facilitating accurate discrimination between stimuli representing threat (Febo et al., 2005). One can also include the preoptic-anterior hypo­
and safety (Janecek and Dabrowska, 2019). Together these neuropep­ thalamic area and associated basal forebrain regions (Stack et al., 2002)
tides have significant influence within this network and jointly modulate in this circuitry (Fig. 5). Data from experimental studies with OT in
complex behaviors such as sexuality, the development of social bonds, particular have supported its vital role in the formation and life-long
and parenting, with effects varying depending on context and the maintenance of pair bonds of the prairie vole (Bosch and Young,
background of the individual (Carter, 2017). 2018). These and similar mechanisms may be biological antecedents to
Some brain structures of the SBNN have been consistently implicated romantic love in humans (Bosch and Young, 2018; Walum and Young,
in social attachment mechanisms in animal models, including pair 2018). OT effects have been linked to behavioral changes that facilitate
bonding and bonding between mother and offspring (Insel and Young, bonding processes such as social salience sensitivity in rhesus monkeys
2001; Stack et al., 2002; Swain et al., 2012). Experimental studies (Parr et al., 2018) and perception of a partner’s responsiveness and
involving damage to the septal region in rodents and gratitude in humans (Algoe et al., 2017). From investigations of

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maternal and romantic love in humans using fMRI, overlapping acti­ dispositional personal distress was associated with greater cortisol
vations in these regions have been reported (Aron et al., 2005; Bartels reactivity to social evaluation stress in mothers, and mother’s ventral
and Zeki, 2004; Swain et al., 2007b). Furthermore, OT receptor poly­ ACC response to positive versus negative child feedback to their
morphisms and prosocial temperament were demonstrated to be asso­ parenting decisions was inversely related to parenting-related cortisol
ciated with individual differences in hypothalamic volume and function reactivity (Ho et al., 2014). Perhaps further work will confirm these
(Tost et al., 2010).2 findings and reveal the directionality of brain and hormone physiology
The social behavior of maternal caregiving (discussed more below in that relate to sensitive parenting and interventions (see 4.3).
4.0) is related to a range of neuroendocrine systems, including OT
(Feldman and Bakermans-Kranenburg, 2017) and cortisol (Swain, 4. Neurobiology of parent-child attachments
2011). In a caregiving study (Elmadih et al., 2016), brain activation to
infant cues was studied among healthy mothers at extremes of the 4.1. Evolutionarily conserved neuroanatomy/systems for response to
maternal sensitivity spectrum. In this study, 15 mothers with the highest infants
sensitivity (HSMs) and 15 mothers with the lowest sensitivity (LSMs)
were selectively recruited from a pool based on mother–infant play One of the landmarks of contemporary developmental psychology
interaction at 4–6 months postpartum. Brain responses to viewing has been its focus on parent-infant attachment (Ainsworth and Bell,
videos of their “own” versus an “unknown” infant in 3 affective states 1970; Bowlby, 1958, 1969; J., 1973) - a universal human phenomenon
(neutral, happy, and sad) were measured at 7–9 months postpartum. The based on the need to form close affect-laden bonds, primarily between
participants’ plasma OT was analyzed immediately following their mother and infant. Attachment is mediated via an innate, evolutionarily
free-play interactions with their infant. HSMs versus LSMs showed conserved psychoneuroendocrinology promoting proximity-seeking
significantly greater brain activation in right superior temporal gyrus between an infant and a specific attachment figure that increases the
(STG) in response to own versus unknown neutral infant and to likelihood of survival to reproductive age. Parental care-giving behav­
own-happy vs. own-neutral (Fig. 6C). Furthermore, the right STG acti­ iors, thoughts and feeling have a predictable time course and charac­
vation in this contrast was negatively correlated with post-free-play OT teristic content (Leckman et al., 2004; Swain et al., 2007b, 2004).
responses in HSMs mothers. The right STG in LSMs was not differentially Current approaches to investigating the human parental brain
activated in response to own infant stimuli. In another example, involve the use of infant stimuli for experimental paradigms that
increasingly address relevant domains of parental function (Barrett and
Fleming, 2011; Swain, 2011; Swain et al., 2007a). A prototypical context
2 for studying the brain basis of parental functions is the naturalistic
Systematic review and discussion of animal model studies of social feelings
mother-infant interaction. This can be approximated in the maternal
is beyond the scope of this paper. The authors recognize, however, that several
key areas of human social feeling research has drawn on animal model studies.
imitation of own vs. other infant facial expressions, which predictably
However, social feelings have been studied in some animal models. For activated their mirror neuron brain circuits, including insula and
example, social disorder models in mice can be linked to human social deficit amygdala according to maternal reflective function (Lenzi et al., 2009).
syndromes, such as autism (Lahvis and Black, 2011; Young et al., 2002) and With an updated child face mirror task, requiring mothers to “empath­
antisocial behavior (Sluyter et al., 2003). Increasing evidence supports that ically join” vs. “observe” own (vs. other’s) child’s joyful vs. distressed
feelings like empathy are also present in animals, including rodents (Atsak expressions, parenting stress was inversely associated with amygdala
et al., 2011; Bartal et al., 2011; Martin et al., 2015; Panksepp and Lahvis, 2011). responses (Ho et al., 2020).
Social recognition in mice is based on olfaction (Bielsky et al., 2004). This is These studies are in accord with the literature on the key role of the
different than social recognition in humans that is more based on visual cues
amygdala and positive feelings in response to own infant face pictures
(Haxby et al., 2002). In rodents, kin recognition, pair bond formation, selective
(Barrett et al., 2012) and maternal-infant biobehavioral synchrony as
pregnancy termination, territoriality and hierarchy depend on the ability to
approximated by using video vignettes as fMRI stimuli for healthy
successfully differentiate olfactory signatures. In rodent social recognition, the
olfactory investigation time decreases with repeated or prolonged contact with postpartum mothers (Atzil et al., 2011). In related work, responses of
conspecifics. Mice deficient in oxytocin fail to develop social memory, and do mothers to videos of interactions with their own 4–6-month-old infants
not remember recently encountered adult animals. This is seen by longer also activated the dorsal anterior cingulate cortex (dACC), fusiform re­
sniffing times, despite normal olfactory abilities (Ferguson et al., 2000). In gion, cuneus, inferior parietal lobule, supplementary motor area, and
studies of social recognition, recognition can be investigated by introducing nucleus accumbens in study participants (Fig. 6A) (Atzil et al., 2014).
mice from another litter and pups from the parents’ own litter to adult male and Furthermore, dACC activation was correlated with mothers’ own
female mice and recording sniffing and licking as a measure for recognition. parent-infant micro-coded synchrony scores. In another brain imaging
Typically, the mice spent more time sniffing the alien pup than the own pup, study aimed at approaching real-life circumstances, Ho et al. (2014)
regardless of the age of pups at testing. Studies of aggressive behavior in mice
reported that maternal neural responses in the amygdala and hypo­
have been undertaken to increase understanding about social conflict and social
thalamus were higher for children’s negative (versus positive) feedback
disorders such as psychosis or borderline personality disorder, in which
aggression plays an important role (Miczek et al., 2001). There is direct evi­
during a decision-making task that involved observing infant suffering.
dence for a modulatory role of various serotonin 5-HT receptors in aggression. Brain responses were related to measures of dispositional personal
The 5-HT receptor modulates dopamine, noradrenaline and glutamate. Play distress, and salivary cortisol stress responses were buffered by activity
fighting, offensive and defensive fighting, maternal aggression and predatory in the social reward circuits of the ventral ACC and connectivity between
aggression exist in rodents. These behaviors are typically analyzed by obser­ hypothalamus and septum – a region important for stress-regulation and
vation and outcome measures like the proportion of animals fighting, tail rat­ empathy (Fig. 6B). In sum, it appears feasible to incorporate naturalistic
tling, chasing, latency for the first-attack bite, and the duration of attack bouts mother-infant interactions within a well-controlled experimental fMRI
or flurries (Miczek et al., 2001). Two behavioral paradigms have been used design to study brain systems that regulate behaviors and feelings.
commonly to study aggressive behavior in rodents. In isolation-induced Parental stress regulation in response to infant distress is a necessary
aggression, a male mouse is singly housed in the home cage for a period of
aspect of sensitive parenting. For example, in response to their infants’
time, after which he is paired with an opponent (Malick, 1979). In the resident
cry, healthy human mothers are likely to pick up, hold and to speak to
intruder paradigm, a male is introduced into the home cage of another male.
Because of territorial instincts, animals do not need to be isolated prior to this their infants - a specific complex of behavioral responsiveness that is
test (Vivian and Miczek, 1993). These animal models increase our under­ known to calm them (Esposito et al., 2013). These behaviors, conserved
standing of the pathways involved in social feelings and to develop behavioral across mammalian species and more than 180 societies, reduce infant
and pharmacological therapeutic strategies to improve the well-being of those crying (Lester and La Gasse, 2008) – supported by a prior randomized
with disorders related to social feelings. controlled trial (Hunziker and Barr, 1986). Perhaps because of their

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Fig. 6. The neurobiology of response to infant stimuli. Most of the literature investigating the neurobiology of mother-child attachment involves mothers watching
scenes or videos of themselves with their children, or videos of their own babies or strange babies in various emotional states (e.g., happy, distressed, neutral). A)
When mothers watched videos of themselves interacting with their own children, fMRI research shows increased activation in the dorsal anterior cingulate cortex,
fusiform gyrus, cuneus, inferior parietal lobule, supplementary motor area, and nucleus accumbens. B) When mothers watched videos of their children, they
generated greater activation in the amygdala and hypothalamus when their child was distressed as opposed to happy. C) Some research has investigated “high
sensitivity” and” low sensitivity” mothers based on plasma oxytocin levels immediately following mother-child play. When shown their own child and a stranger’s
child in neutral, happy or sad states, high sensitivity mothers displayed increased activation of the right superior temporal gyrus when their own child was happy
compared to neutral. This was not seen in low-response mothers.

evolutionary advantage, as highlighted indeed by Darwin (Darwin, month postpartum, but not at 3–4 months postpartum, were associated
1872), reactions toward infants distress are specific and automatic, with lower child socio-emotional competencies at 18–24 months post­
widespread culturally, and embedded neurobiologically in mothers – partum. Maternal neural responses in motor cortex and substantia nigra
and connected to parenting feelings. For example, human parents have were positively and negatively associated with their anxious thoughts
specific implicit cognitive (Senese et al., 2013), autonomic (Esposito and actions, respectively. In fathers, a more positive perception of being
et al., 2014, 2015), and brain (Caria et al., 2012) reactions to human a parent during the first month postpartum, but not at 3–4 months
infant faces that differ from their responses to faces of human adults and postpartum, was associated with higher socioemotional competencies in
faces of infrahuman mammal infants and adults. Recent study also toddlers at 18–24 months postpartum. Paternal neural responses in
confirmed that picking up and holding their infants are preferential auditory cortex and caudate were also positively associated with their
maternal social caregiving behaviors across 11 countries and showed positive thoughts, perhaps because of enhanced sensory information
brain imaging evidence for common responses to infant cry in brain processing. Although awaiting replication, this work implicated certain
circuits that regulate the intention to move and speak across 3 cultures parent brain regions associated with very early postpartum parental
(US, China and Italy) (Bornstein et al., 2017). thoughts and behaviors that potentially relate to their infant’s future
socioemotional outcomes. Possible sex differences and treatment im­
4.2. Affective neurocircuitry for mothers and fathers that connects to plications in these findings require further research. A potential role for
child outcome social feelings within parenting roles may be an important intervening
variable that can be influential in shaping child outcomes (e.g., stress
Recent research has begun to investigate how sensitive parenting and buffering) and conducive to modification in order to improve such
parental brain physiology in the first few postpartum months related to outcomes.
later child development (Kim et al., 2015b). In this study, associations Exploring the potential similarities and differences between
between parental thoughts/actions and brain responses to baby-stimuli mothers’ and fathers’ parenting-related feelings and brain function
in mothers and fathers in the neonatal period were studied in relation to constitutes another promising direction of parental brain research (Ril­
the child’s social and emotional development at toddler age. Mothers (n ling and Mascaro, 2017; Swain et al., 2014). Building on similar research
= 21) and fathers (n = 19) were scanned while they listened to their own in mothers, changes in fathers’ brain structure using voxel-based
and unfamiliar baby’s cry in the first month postpartum. Mothers’ morphometry analysis (n = 16) have been reported from 2 to 4 to
higher levels of anxious thoughts/actions about parenting in the first 12–16 weeks postpartum (Kim et al., 2014a). Fathers exhibited an

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increase in gray matter volume (GMV) in several brain regions puta­ to childhood poverty and other parental stress. For example, childhood
tively involved in parental motivation, including the hypothalamus, poverty impacts parents – and interestingly in a sex-specific manner in
amygdala, striatum, and lateral prefrontal cortex. Conversely, fathers the brain (Kim et al., 2015a). In females, childhood poverty was asso­
exhibited decreases in GMV in orbitofrontal cortex (OFC), posterior ciated with increased neural activations to infant cry in the posterior
cingulate cortex, and insula. The findings suggest that neural plasticity insula, striatum, calcarine sulcus, hippocampus, and fusiform gyrus, but
in fathers’ brains may be distinct from those of mothers reported pre­ with decreased neural responses to infant cry in the same regions in
viously (Kim et al., 2010). males (Fig. 7A). Furthermore, neural activation in these regions was
associated with higher levels of perceived annoyance elicited by infant
cries and reduced motivation to approach crying infants regardless of
4.3. Parental affective neuroscience informed by psychopathology, stress, the gender of the participants (Kim et al., 2015b). This work underlines
and interventions the need for special attention to the paternal brain as mentioned above.
In a related study (Kim et al., 2016), lower income was associated with
Parental stress and mood symptoms are issues of high concern given reduced responses to infant cry in brain circuits that are thought to
the impact on child development. Mother’s amygdala activity may be evaluate emotional valence (medial prefrontal gyrus), regulate affect
hypo-responsive to certain standard cognitive neuroimaging challenges (middle prefrontal gyrus) and process sensory information (superior
(Moses-Kolko et al., 2014) with depression and unresolved attachment temporal gyrus). Furthermore, lower positive perceptions of parenting
trauma after viewing their own (but not unknown) infant’s crying faces were associated with reductions in infant-cry response in the right
(Kim et al., 2014b). With a child face empathy task, depressed compared middle frontal gyrus and superior temporal gyrus.
to healthy mothers displayed greater reactivity of the right amygdala, Characterization of parental brain function and dysfunction may also
which was interpreted as emotional dysregulation (Lenzi et al., 2016). be informed by neuroimaging before and after parenting treatment such
Finally, amygdala reactivity was increased in a self-focused baby-cry as the Mom Power (MP) intervention, which aims to promote maternal
task designed to provoke brain responses in participants with a history of empathy, reflective functioning, and stress reduction skills (Muzik et al.,
adverse early life experiences, sometimes described as a malevolent 2015, 2017). In one study, MP treated mothers, as compared to un­
background “shark music” (Ho and Swain, 2017). These data support treated mothers, showed decreased parenting stress and increased
the hypothesis that amygdala response to infant stimuli is a function of child-focused responses in social brain areas highlighted by the pre­
the personal relevance of the stimuli. Variance in the properties of infant cuneus and its functional connectivity with subgenual ACC – key com­
stimuli and context of presentation, along with research using hormone ponents of social cognition. Furthermore, time-dependent reduction in
challenges may be helpful in clarifying the role of the amygdala in parenting stress was related to concomitant increased child- vs.
depression – especially given that often-used depression measures may self-focused baby-cry responses in amygdala-temporal pole functional
not perfectly capture real-life parental dysfunction. For example, intra­ connectivity, which may facilitate maternal ability to take her child’s
nasal OT effects on amygdala response to infant crying was found to be perspective (Swain and Ho, 2017) (Fig. 7B). Finally, MP significantly
moderated by attachment security of mothers, with OT decreasing increased maternal empathy-dependent amygdala responses for own
emotional and amygdala reactivity only in mothers with insecure versus other child’s joyful expressions (Ho et al., 2020). Another inter­
attachment representations (Riem et al., 2016). Thus, parents with vention, Attachment and Biobehavioral Catch-up (ABC), was associated
insecure attachment, perhaps different from other attachment classifi­ with larger increases in event related potential responses to emotional
cations and with different social feeling states, may have different brain faces relative to neutral faces, which in turn was associated with
mechanisms that render them amenable to OT interventions. observed maternal sensitivity (Bernard et al., 2015) and greater
Recently, parental brain studies have begun to report findings related

Fig. 7. Parental affective neuroscience and response to infant stress. Parent-child relationships – like any relationship – are influenced by outside factors, such as
previous childhood poverty experienced by the parents. A) Response to a distressed child shows sex-specific brain activation in parents who had experienced
childhood poverty. Specifically, women show increased activity in the posterior insula, striatum, calcarine sulcus, hippocampus, and fusiform gyrus, whereas men
show decreased activation in these regions in response to infant cries. These neurobiological changes were associated with self-reported feelings of annoyance and
reduced desire to approach infants in both men and women. B) Intervention, such as training programs for promoting maternal empathy and learning stress reduction
skills (called “Mom Power”), was shown to increase activity in typical child-focused, social brain areas like the precuneus, subgenual anterior cingulate cortex, and
amygdala-temporal pole functional connectivity. This training and altered brain activity was accompanied by decreased annoyance and stress felt by mothers.

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responses for ~10 year olds to own mother picture cues in social century, Welt concluded that damage to the right medial orbital region
cognition regions: precuneus, cingulate, and hippocampus (Valadez was necessary to produce a change in moral character in a neuropath­
et al., 2020). Behavioral and brain imaging parameters of parental stress ological case series (Zahn et al., 2015). In the 1980s, Eslinger and
and empathy are also disturbed for mothers with substance use disorders Damasio (1985) stimulated new interest in the neuroanatomy of the
such as the current epidemic of opioid use disorder. Opioids may ventromedial frontal cortex (FC) by describing EVR, a patient with
modulate the maternal caregiving or behavior neurocircuits (Swain and impaired moral and social behaviour. Around the same time, it was
Ho, 2019, 2021; Swain et al., 2019) – as developed from non-human shown that frontotemporal dementia (FTD), particularly behavioural
research (Klein et al., 2014; Numan and Woodside, 2010). Such neu­ variant FTD (bvFTD) which regularly affects ventral frontal regions, can
rocircuits are hypothesized to govern human maternal behavior via two be diagnosed before death based on clinical features and was more
reciprocally modulating subsystems. These inhibit each other to either common than originally thought (Snowden et al., 2001). Patients with
activate maternal caregiving behaviors when solicited by the infant or FTD display impaired social behaviour (Bozeat et al., 2000). This was
aggressive behaviors when the infant is threatened. Elucidating these not only correlated with ventromedial FC, including the subgenual re­
and related mechanisms that could lead to more specific and effective gion, but also right anterior temporal lobe (ATL) damage (Liu et al.,
treatments. 2004). Ventromedial FC lesions that included subgenual sectors of the
Thus, parenting may be conceptualized as a specific instance of OFC were associated with a lack of guilt reported by caregivers (Koenigs
altruistic social feelings that may positively influence health-related et al., 2007). A study using fMRI and lesion information from patients
outcomes and is amenable to intervention (Brown and Brown, 2015; with FTD showed that the ventromedial FC relates to the anticipation of
Ho et al., 2021; Konrath et al., 2015; Swain et al., 2012). Taken together, negative consequences of social behaviour (Grossman et al., 2010),
these results suggest that enhancing child-oriented altruistic social which is an important pre-requisite for experiencing guilt.
feelings may protect mothers from adverse effects of distress and stress Septal damage in FTD was associated with diminished guilt and pity,
related to caregiving - consistent with the hypothesis that prosocial but not embarrassment in an experimental task, whilst frontopolar
motivation improves caregivers’ well-being (Brown and Brown, 2015). damage was associated with impaired embarrassment in addition to
guilt and pity (Moll et al., 2011). This showed that septal damage was
5. Moral sentiments as social feelings: neural considerations associated with impairments of those moral feelings that entail empathic
concern for other people, whilst frontopolar cortical damage was asso­
5.1. History and definition of moral sentiments ciated with prosocial feelings more generally, including embarrassment
which is primarily related to upholding one’s social reputation rather
Francis Hutcheson, his successor Adam Smith, and David Hume than concern for others (Eisenberg, 2000). In contrast to these associa­
(Zahn et al., 2011b) highlighted the central importance of moral senti­ tions of different moral feelings with different frontal-subcortical lesion
ments for moral behaviour. Adam Smith conceived “sympathy”, as patterns, another study showed that FTD patients with right ATL dam­
“man’s capacity for fellow feeling with others”, and considered it the age displayed selective impairments of abstract social relative to
most important moral sentiment (Lamb, 1974). Hutcheson stated that non-social conceptual knowledge (Zahn et al., 2009b) irrespective of the
“benevolence” motivates virtuous actions and thereby provides “moral attached emotional valence. These lesion studies confirmed earlier fMRI
motivations” (Bishop, 1996). Modern authors use the term “moral evidence of partly dissociable representations of abstract conceptual
emotions” rather than “moral sentiments”. There is some disagreement social knowledge in the right superior ATL (Zahn et al., 2007) and
about which emotions are considered moral (Eisenberg, 2000; Tangney different moral feelings in frontal-subcortical regions (Zahn et al.,
et al., 2007a). Immanuel Kant, a contemporary of Hume, distinguished 2009c), which can independently contribute to impaired prosocial
the ability to judge what is morally right and wrong (“principium behaviour (Krajbich et al., 2009; Liu et al., 2004). Finally,
diiudicationis”) from the motivation (“principium motivationis”) to act meta-analytical evidence suggests that when frontomedian cortex is
accordingly (Kant, 1786; Zahn et al., 2015). He was opposed to the affected in bvFTD, it is associated with moral and social cognitive im­
notion that moral actions could be defined on the basis of experienced pairments. Analyses of empathic deficits in bvFTD have additionally
moral sentiments, which he considered as originating from the external identified pathology in the anterior insula and anterior cingulate regions
senses. Instead he claimed that true moral actions are motivated directly (Schroeter et al., 2015, 2014).
by respect (“Achtung”) for the moral law, which is self-generated and an
act of free will (Kant, 1786). Thus, moral motivations as defined by the 5.3. Imaging the experience of moral feelings
opposing schools of moral philosophy are either the respect for moral
rules (Kant) or moral sentiments (Zahn et al., 2011a). Neuroscience and The investigation of the neural correlates of subjective experiences of
psychology research allows for developing theories and generating ev­ moral feelings in healthy people using fMRI has led to a number of
idence about the structure and dynamics of subjective experiences and interesting findings but can only be interpreted in light of brain lesion
behavioural expressions of moral motivations, such as “respect for moral evidence. This is because fMRI also displays brain regions that likely are
principles” or “feelings of guilt”, and their neural underpinnings. unnecessary for a given task or stimulus representation and merely
We use the terms “moral sentiments” and “moral feelings” synony­ reflect uncontrolled differences between experimental conditions.
mously, stressing the subjective and complex nature of moral sentiments Here, we focus on guilt and pity/compassion, given that the body of
which include cognitive ingredients such as causal attributions. evidence on other moral sentiments is not large enough yet to draw
As recently reviewed (Zahn et al., 2020), although moral feelings conclusions. The anticipation of guilt is important in preventing moral
have probably developed from affiliative feelings more generally, they violations and to motivate reparative actions (Eisenberg, 2000; Tangney
are a distinct subset in that they enable humans to be motivated by other et al., 2007a). Empathic concern is an essential ingredient of empathy­
people’s or societal needs in the absence of benefits to oneself or one’s —and is closely related to pity, sympathy, and compassion (Weng et al.,
kin. 2015). Such feelings extend beyond perceiving, sharing or simulating
other’s emotions (e.g. sharing pain which is associated with anterior
5.2. Brain lesions and impaired moral sentiments insula and dorsal cingulate brain activation (Lamm et al., 2011),
requiring an extra step of feeling for the other person (de Vignemont and
By demonstrating which brain regions are necessary for moral and Singer, 2006; Decety et al., 2012). Frontal polar cortex activations
prosocial behaviour, lesion studies provide important insights, even if emerge as most reproducible for both guilt (Basile et al., 2011b; Kedia
they relate to less confined anatomical areas and in some instances have et al., 2008; Moll et al., 2007; Morey et al., 2012a; Seara-Cardoso et al.,
to infer sentiments from observed behaviour. Already in the 19th 2016; Takahashi et al., 2004; Zahn et al., 2009c) and compassion (Fehse

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et al., 2015; Ho et al., 2021; Immordino-Yang et al., 2009; Kedia et al., inquiry, is to consider studies that directly induce real or imagined
2008; Moll et al., 2007) compared against equally unpleasant and interpersonal stress (i.e., the presence of conflict or threat, or the loss or
complex emotions, such as indignation towards others. In addition, guilt absence of belonging or connection) and ask participants to provide
was reproducibly associated with activations of the subgenual cingulate ratings for their emotional feeling states (Coan and Sbarra, 2015).
cortex (extending posteriorly to the adjacent septal area and the more Current understanding of the central neurobiology of social feelings in
anterior pregenual cingulate area in several studies) when compared this context is limited because such studies have been dominated by a
with other complex negative emotions (Basile et al., 2011b; Green et al., focus on peripheral physiology. However, this area provides unique
2012; Morey et al., 2012a; Zahn et al., 2009a,c). Septal and/or sub­ opportunities to investigate social feelings in the context of integrated
genual cingulate activations for guilt were reported in several studies, brain-body pathways.
however, only when modelling individual differences in guilt proneness A relevant meta-analysis of studies that induced unpleasant feeling
and empathic concern (Green et al., 2012; Zahn et al., 2009a,c). states using ecologically valid approaches (e.g., public speaking, marital
Despite these reproducible associations of subgenual cingulate and conflict, films, music, mental re-experiencing) and measured peripheral
septal activations with individual differences in guilt-proneness and stress, linked these physiological parameters to inferred feeling states
empathic concern, two recent systematic reviews of fMRI studies prob­ (Denson et al., 2009). Specifically, nine judges were asked to mentally
ing guilt (Bastin et al., 2016; Gifuni et al., 2016) have failed to detect imagine themselves in the participant’s position and rate the intensity of
these regions. The reviews did not base their conclusions on studies feelings they imagined the stressor in each study would have provoked,
controlling for individual differences in the experience of guilt-evoking including social feeling states (e.g., submissive, fear of losing social
stimuli, nor on those studies using optimised fMRI sequences for ventral approval, ashamed, guilty, embarrassed) (Fig. 9A). These ratings were
frontal regions. It is not surprising, therefore, that subgenual cingula­ then used to predict effect sizes for stress-induced changes in biological
te/septal activations were not emphasized. This will be important in mediators. Statistically significant effects were observed for three of five
future systematic reviews. social feelings. Stronger feelings of submissiveness and fears of losing
social approval (as rated by the judges) predicted greater stress-induced
increases in the endocrine hormone cortisol, an end-product of
5.4. Converging evidence from fMRI and lesion studies on moral hypothalamic-pituitary-adrenal axis activation (Fig. 9B). Stronger feel­
sentiments ings of embarrassment predicted greater stress-induced decreases in
T-lymphocyte numbers, indicating a potential dampening of immunity
To summarise, lesion and fMRI data point to an important role for the (Fig. 9C). In contrast, two of the eight other feelings (i.e., surprise and
septal region and ventromedial parts of the frontal cortex, in particular anticipation of a social encounter) showed statistically significant ef­
its subgenual cortex (BA25) component and the more anterior subgenual fects, predicting increases in cortisol and decreases in T-lymphocyte
cingulate cortex, in processes of guilt and compassion (Fig. 8). Lesions to numbers, respectively.
other cortical brain regions which were shown to represent goals of This meta-analysis revealed an important role for social feeling states
socio-moral behaviour, such as long-term consequences (frontopolar in peripheral stress physiology, especially feelings that arise when social
cortex, (Wood and Grafman, 2003) and conceptual quality of social status is threatened, and especially when compared to “fight-or-flight”
behavior (right superior ATL, (Zahn et al., 2009b) led to changes in feelings that are often the focus in studies of stress. In addition, it
moral behavior as well (Zahn et al., 2009b) (Fig. 8) in keeping with the highlighted the variety of experimental approaches used to study social
notion that moral behavior requires both socio-emotional qualities such feelings under interpersonal stress. This raises an important question: Do
as “affiliation” that have important elements of social feeling and the social feelings and their underlying neural processes depend on different
goal representations to which those sentiments are attached (Moll et al., aspects of the experimental manipulation? This question is at the heart
2008a). of the emerging area of second-person neuroscience (Redcay and
Schilbach, 2019). The premise of this area is that the neurobiology of
6. Neurobiology of social feelings under interpersonal stress social processing varies as a product of two interpersonal dimensions:
emotional engagement and interaction (Schilbach et al., 2013).
A useful way to investigate whether social feelings are a naturally The emotional engagement dimension refers to the degree to which
occurring neurobiological kind, identifiable and conducive to scientific social stimuli are processed as self-directed and self-relevant (more
emotional engagement), as opposed to from an observer’s perspective
(less emotional engagement). Neuroimaging studies suggest that the
affective and rewarding components of emotional engagement are
particularly linked to the amygdala, the ventral portion of the medial
prefrontal cortex (mPFC) (Schilbach et al., 2006) the temporo-parietal
junction (Redcay et al., 2010, 2013) and striatal structures. The inter­
action dimension refers to the degree to which one is involved in a real
or imagined interpersonal exchange (structured or dynamic), as opposed
to being a passive observer of social stimuli (Krach et al., 2013; Schil­
bach et al., 2013). During direct interactions the mPFC, the posterior
superior temporal sulcus and precuneus as parts of the mentalizing
system as well as the anterior insula and ACC as part of a sharing system,
are thought to be involved when we make sense of others’ states in the
transition from social isolation to interpersonal exchange. Still very
preliminary findings reveal evidence for greater activation of, and in­
teractions among the mentalizing/sharing system and affect coding/­
reward networks (Redcay et al., 2010; Redcay and Schilbach, 2019, p.
Fig. 8. Regions associated with empathy, as informed by lesion and fMRI
497) as participants move from processing social information that is low
studies. Feelings of guilt and compassion are strongly associated with typical
functioning of the subgenual/septal region and ventromedial frontal cortex. on emotional engagement and interaction versus high on emotional
Longer-term emotions, such as processing long-term consequences and engagement and interaction. Further, it has been proposed that the
conceptualizing quality of social behavior, activate the frontopolar cortex and mental state and neural qualities that are triggered by emotionally
the right superior anterior temporal lobe. engaged interactions—termed “social immersion”—may persist after

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Fig. 9. Interpersonal stress and peripheral

physiological responses. The physiological
response to interpersonal stress has been
investigated using a design where people were
asked to “judge” another while imagining them
in the judged-person’s position and rate their
social feelings and “other” feelings. A) Social
feelings assessed included i) submissiveness, ii)
fear of losing social approval, iii) shame, iv)
guilt, and v) embarrassment. B) Judges’ ratings
of the other person’s feelings of submissiveness
and fear of losing social approval predicted a
larger increase in the judged person’s cortisol
levels. C) Judges ratings of the other person’s
feelings of embarrassment predicted a decrease
in T-lymphocyte numbers.

the social interaction ends (Krach et al., 2013, p. 427). Overall, this positive, and negative evaluative “social feedback” trials by viewing a
implies achieving clarity about the neurobiology of social feeling states cursor periodically selecting various adjectives (e.g., serious, shallow);
will require teasing apart factors that differentially engage these two they were led to believe that this feedback reflected the other person’s
interpersonal dimensions (i.e., emotional engagement and interaction). impression of them based on the video recording. From the perspective of
second-person neuroscience, this social-evaluative stressor can be char­
6.1. Social-evaluative threat acterized as high on emotional engagement (self-directed and -relevant),
but low on social interaction. However, the paradigmatic set-up let par­
Grounded in animal models of social subordination stress, social- ticipants immerse into the situation rendering the mental representation of
evaluative threat is a specific type of interpersonal stressor that in­ oneself in relation to the evaluating other as essential. Exposure to the
volves potential loss of social status or social regard (Kemeny, 2009). social feedback trials in aggregate (i.e., all neutral, positive, and negative
Exposure to acute social-evaluative threat (e.g., solving math problems, trials) increased momentary feelings of social rejection and evaluation
estimating properties of a stimulus or giving a speech in front of a panel from before to after the scanning session, along with plasma levels of the
of deadpan evaluators) involves high emotional engagement in the cytokine interleukin-6 (IL-6), an immune system cell that has actions that
context of a structured social interaction. Especially by manipulating the promote inflammation. However, increases in social feelings and in IL-6
presence or absence of a judging audience, participants are motivated to levels were not correlated. Moreover, these two responses were differen­
think about others’ evaluations and how one’s performance might affect tially related to neural activity during negative vs. neutral social feedback
the impression others will have of them. In studies of social-evaluative trials. Increases in momentary feelings of rejection (but not evaluation)
threat that include measures of emotional states, participants are typi­ were related to heightened activity in neural regions engaged by self- and
cally asked to rate momentary feelings (i.e., “How do you feel right social-processing, including mentalizing (i.e., mPFC, posterior cingulate
now?”) immediately before and after the experimental manipulation. cortex, and hippocampus). Increases in IL-6 levels were related to
Compared to participants assigned to solve math problems, estimate heightened activity in neural regions engaged by affective/threat-related
properties or give a speech either alone or with the mere presence of an processing (i.e., amygdala), and to greater functional connectivity be­
inattentive person without any evaluation (Guerin, 1986), participants tween these regions and mentalizing-related regions (i.e., dorsomedial
exposed to a judging audience showed greater increases in the endocrine prefrontal cortex) (Muscatell et al., 2015; Muscatell and Eisenberger,
stress hormone cortisol (Kirschbaum et al., 1993), along with the 2012) (Fig. 10A). This study provides a preliminary look at the neural
momentary feelings of shame and related feelings (e.g., humiliated, correlates of momentary stress-related social feelings under
foolish) (Dickerson et al., 2008; Gruenewald et al., 2004) or embar­ social-evaluative threat. However, specificity for social feelings cannot be
rassment (Muller-Pinzler et al., 2015). Social feelings were accompanied determined because other feelings were not assessed.
by increases in salivary cortisol (Dickerson et al., 2008; Gruenewald This issue was addressed in an fMRI study in which participants
et al., 2004) or pupil diameter as a correlate of affective arousal (Mul­ received false negative, neutral and positive feedback about their cogni­
ler-Pinzler et al., 2015), and persons who reported greater increases in tive estimation performance both privately and publicly. Specifically, in
shame-related feelings (but not anxiety or fear) showed the greatest the public condition, participants were led to believe that three other
increases in cortisol. persons whom they had met prior to entering the scanner, and who
Studies that induce social-evaluative threat using stressors that can be remained seated adjacent to the scanner during the entire session, could
manipulated within the confined set-up of an fMRI have begun to address observe the feedback about the estimation performance given to the
the central neurobiology of social feelings induced by social-evaluative participants inside the scanner. In the private condition, estimation feed­
threat. Mostly, these studies utilize cover stories or staged interactions backs were not projected outside to the audience (Muller-Pinzler et al.,
with confederates to create ecologically valid social contexts. In one such 2015). The feedback and private-public manipulation were delivered on a
study, participants discussed their positive and negative qualities while computer screen immediately following each cognitive estimation trial.
being videorecorded (e.g. “What are you most proud of?”); they were led After scanning, participants reported their social feelings (embarrassment,
to believe that another person (i.e., a confederate to whom they had been pride) and other feelings (anxiety, anger, sadness, happiness) for each trial
introduced prior to scanning) would view the recording in order to form type. The feeling of embarrassment was most affected by negative feed­
an impression of them (Muscatell et al., 2015). Subsequently, and while in back (failure) that was observed by others (publicity), the two defining
the scanner, participants were exposed to a combination of neutral, factors of embarrassment (Miller, 1996). Sympathetic nervous system

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Fig. 10. Neurobiology of interpersonal stress.

Participants in these studies were asked to
discuss their positive and negative qualities on
video; they were then placed into a scanner,
where they received “social feedback” from
another person watching their video, which
indicated adjectives such as serious or shallow.
A) Greater release of the cytokine IL-6 was seen
following trials, regardless of feedback type.
Increased activity in the medial prefrontal cor­
tex, posterior cingulate cortex, and hippocam­
pus was observed when subjects reported
increased momentary feelings of rejection, as
well as increased activity in the amygdala and
functional connectivity between the amygdala
and dorsomedial prefrontal cortex. B) Another
study examined responses to negative, positive,
and neutral feedback given publicly or pri­
vately. This research led to the identification of
the “Embarrassment Pathway,” which was most
affected by negative feedback. This includes
regions for processing the feedback, such as the
dorsal anterior insula, processing the publicity,
such as the medial prefrontal cortex and pre­
cuneus, and connectivity of these regions
involved in affect processing, such as the
amygdala and ventral anterior insula. These
were also associated with increased pupil
dilation.

arousal, indexed by pupil dilation, was also greater during the public presence/absence of the audience and accompanying positive evaluation
versus private feedback and, while also increased during positive feed­ of others (Muller-Pinzler et al., 2015). Rather than being affected by the
back, the interaction of failing in public was associated with the strongest publicity manipulation, pride feelings seem to depend on internal control
pupil dilation. Further, during negative versus positive feedback, brain beliefs when performing a task (Stolz et al., 2020). Further research might
regions that were involved in processing negative feedback and related also reveal that different neural systems underlie the experience of
arousal (dorsal anterior insula), and those that were involved in mental­ authentic, positive pride and the more negative hubristic pride associated
izing about the publicity (mPFC and precuneus), both showed greater with arrogance and contempt.
functional connectivity with core affective processing regions (amygdala
and ventral anterior insula) (Adolphs et al., 1995; Kelly et al., 2012)
6.2. Social exclusion
(Fig. 10B). Based on this pattern, the authors concluded that the integra­
tion of arousal, mentalizing, and affective/threat-related processing sys­
Social exclusion (also referred to as ostracism or social rejection) is a
tems forms a “neural pathway of embarrassment” (Muller-Pinzler et al.,
type of interpersonal stress that has received attention because of the
2015, p. 252). On the other hand, if the focus was on being successful
centrality of social connections in human health and survival (Eisen­
during the cognitive estimation task, the experience of pride feelings was
berger, 2012). The neurobiology of social exclusion has often been
associated with increased activation of the brain’s reward circuits in the
studied using a virtual ball-tossing game (i.e., cyberball). From a
striatum (Muller-Pinzler et al., 2015). As shown also in other studies, pride
second-person neuroscience perspective, this approach involves
is elicited when humans achieve self-relevant goals. Studies suggest that
emotional engagement (i.e. self-relevance and self-directedness) and the
its social function relates to the signaling of (real or imagined) status with
sense of being involved in a social interaction (i.e. receiving and passing
potentially beneficial effects for both the displayer and observers (Bollo
on of ball tosses). However, to induce the experience of social exclusion
et al., 2018; Martens et al., 2012). Accordingly, on the neural systems
it is necessary to make participants believe and immerse into the set-up
level, the mPFC and precuneus, areas of the mentalizing network, are also
of social interaction. The typical feelings measured using this approach
implicated during pride experiences when participants reflect about their
are those of momentary “social distress”. Social distress is a composite
behavior and their evaluation in the eyes of others (Takahashi et al., 2008;
that includes social feelings such as rejection, disconnection, not
Williams and DeSteno, 2008; Zahn et al., 2009c). However, according the
belonging, not liked, invisible, but also other feelings related to
mentioned study, the variability of pride was less affected by the
self-esteem and control that area less socially focused (Williams, 2009).

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These “painful feelings associated with social disconnection” have also dorsomedial prefrontal cortex, posterior cingulate cortex, and pre­
been described as “social pain” (Eisenberger, 2012, p. 421). In numerous cuneus. Although the IAT was performed in social isolation, the expe­
studies, greater activity in various subregions of the ACC in response to rience of guilt may have involved ongoing thoughts about one’s own
social exclusion versus inclusion correlated positively with momentary actions that caused harm to another person or group of people. Thus, it is
feelings of social distress, with ACC subregion involvement being not surprising that most studies found evidence for guilt-related acti­
influenced by a variety of methodological factors (Eisenberger et al., vations of mentalizing areas, such as mPFC, posterior cingulate cortex,
2003; Rotge et al., 2015). In addition, greater ACC activity during social and precuneus (Basile et al., 2011a; Fourie et al., 2014).
exclusion, along with greater amygdala and periaqueductal gray activ­ Another study employed a more interpersonal approach to induce
ity, correlated positively with momentary feelings of social distress in guilt in the MRI and studied guilt-associated reparative behavior (Yu
response to social interactions in the natural environment (Eisenberger et al., 2014). Participants played an interactive game with an alleged
et al., 2007a). Further, activation of hippocampus and mPFC regions anonymous partner and were punished with painful stimulation when at
during social exclusion correlated positively with greater correspon­ least one of them responded incorrectly. In this case, participants were
dence between momentary social distress in the natural environment given the option to bear a portion of pain that would otherwise be
and feelings of social distress as persons reflected over their day delivered to the partner. Trials in which participants were solely
(Eisenberger et al., 2007a). From the perspective of second-person responsible for the punishment elicited greater feelings of guilt, a higher
neuroscience, this pattern supports the hypothesis that persons who sense of responsibility, higher levels of distress and higher willingness to
processed lab-based social exclusion with greater emotional and inter­ receive a portion of the partner’s pain, as compared to trials in which
personal engagement were more prone to translate this experience of both partners were responsible for the punishment. These trials were
social distress to everyday life social interactions in the natural further associated with activity of dorsal ACC and insula, again
environment. demonstrating the involvement of paralimbic regions in guilt states.
In a different approach, voluntarily reliving a socially painful inter­
personal stressor (e.g., a break-up, exclusion, or betrayal) as compared to a 6.4. Resilience
neutral interpersonal event, and as compared to a physically painful versus
physically neutral event, was associated with greater activity in the dorsal Finally, there is preliminary evidence that social feelings with posi­
anterior cingulate cortex (dACC) and anterior insula. The stronger feelings tive valence may confer neurobiological resilience to interpersonal
of social pain evoked by reliving interpersonal stress versus physical pain stress. In an observational study, reports of more social interactions over
correlated positively with greater dACC activity. Further, the overall 10 days with persons generally perceived as closer, more comforting,
pattern reflected enhanced mentalizing, or processing of one’s own and and more supportive were associated with less dACC activity during
others’ mental states, during reliving of interpersonal stress versus phys­ laboratory-based social exclusion vs. inclusion. This lower dACC activ­
ical pain, as indicated both imaging data (i.e., greater activity in the dorsal ity, in turn, was associated with lower cortisol responses to laboratory
mPFC) and behavioral data (i.e., more indicators of mental state pro­ social-evaluative threat (Eisenberger et al., 2007b). In an experimental
cessing in participants’ written descriptions of the stressor) (Meyer et al., study, the effectiveness of three interventions for reducing feelings of
2015). Another study showed that the secondary somatosensory cortex - anxiety and peripheral stress mediators (cortisol, markers of inflam­
an area usually involved in coding the sensory component of physical pain mation, and indicators of autonomic nervous system (ANS) activity) in
- was activated by the mere re-imagination and reliving of a romantic response to acute social-evaluative threat was assessed: dyadic training
partner break-up triggered by viewing a headshot photograph of the in cultivating positive social feelings (compassion, kindness, gratitude),
ex-partner (Kross et al., 2011). dyadic training in cultivating cognitive perspective-taking on self and
others, and individual training in focused attention and interoception
6.3. Interpersonal transgressions (Engbert et al., 2017). The two dyadic trainings were motivated by ev­
idence that rather distinct neural networks—empathy and mentalizing,
An intense aversive social feeling state that arises when we believe respectively—are involved in these two modes of interpersonal under­
that we have behaved immorally or transgressively is guilt. Although standing (Kanske et al., 2015). Compared to a no-treatment control, all
guilt may also initially emerge in social isolation, its unpleasantness is interventions reduced feelings of anxiety in response to social-evaluative
mostly related to thoughts about the harm that one has caused to others threat. None of the interventions reduced inflammatory or ANS re­
and the fear of consequent rejection (Baumeister, 1994). Guilt thus in­ sponses to social threat. In contrast, dyadic training in cultivating pos­
volves an involuntary transgressive part, which then usually is followed itive social emotions, and dyadic training in cognitive
by an approach-oriented and reparative part to fix the unpleasant situ­ perspective-taking when combined with individual training in focused
ation (Fourie et al., 2012, 2014; Tangney et al., 2007b). While most attention and interoception, both reduced cortisol responses to social
neuroscience studies on guilt used script-based approaches and mental threat compared to the no-treatment control. The authors speculated
imagery (Basile et al., 2011a; Morey et al., 2012b; Shin et al., 2000; that training in cultivating positive social feelings and social
Takahashi et al., 2004), Fourie and colleagues used a clever set-up to perspective-taking may build resilience to the shame response that is
directly induce states of guilt within the fMRI. To do so, they invited provoked by social-evaluative threat (Engbert et al., 2017). Unfortu­
participants to a study allegedly examining prejudices among college nately, however, measures of social feelings were not reported.
students. Participants were told that they had been selected based on Overall, this emerging picture suggests that the neurobiology of so­
their overall positive explicit attitudes toward most social groups, but cial feelings ranging from concerns about social belonging and poten­
that there is usually a significant discrepancy between what people say tially diminished value in the eyes of others (i.e., submissiveness, loss of
they feel, and what they really feel, toward these groups. Participants approval, shame, guilt, embarrassment, composite social distress)—or
subsequently performed an implicit association task (IAT) with neutral what might be termed lower “relational value” (Leary, 2015, p. 435)—
(sports, hair), positive (weight, religion) and negative (race, sexuality) to positive social feeling states such as pride, compassion or gratitude
response categories in the scanner. A preprogrammed feedback elicited may play a key role in interpersonal states, even when compared to more
guilt by providing participants information that contradicted their belief basic emotions or feeling states that have traditionally been the focus in
that they held egalitarian attitudes toward Black and phys­ such studies. This evidence lends support to the idea that “social feel­
ically/intellectually disabled people. The fMRI data indicated that this ings” might be a neurobiological natural kind that is identifiable and
unpleasant feeling of guilt was associated with increased activity in conducive to scientific inquiry. Consistent with ideas from
anterior paralimbic structures, including the ACC and anterior insula, second-person neuroscience, results generally highlight the role of brain
but also extended to areas associated with mentalizing, including the regions involved in emotional engagement (affective and reward-related

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structures) and interaction (sharing and mentalizing related structures) difficult to draw conclusions about integrated brain-body pathways.
in social feelings, although this varies by the specific paradigm for However, given that interpersonal stressors are among the most conse­
inducing interpersonal emotions, and by how and when social feelings quential stressors for health (Holt-Lunstad et al., 2017; Liu et al., 2017;
are measured. Resnick et al., 1993), such approaches may yield important information
Recommendations for future research include measuring a range of about the role of social feelings in homeostasis and overall health.
social feeling states, and teasing apart composite measures of social
distress, to ensure that results are specific to social feelings. This is 7. Neuroscience of Social Feelings associated with emotional
particularly important given that neural regions may be involved in communications
processing multiple feelings (e.g., Eisenberger, 2015). Measuring feel­
ings both before and after stressors (or in response to different trial Affective states are communicated overtly through physiological
types) will also be important to ensure that any observed neural corre­ (blushing, sweating), behavioral (body posture, facial expression,
lates are linked to stress-induced social feelings, rather than to stable modulation of the voice, interjections), and verbal (“I am really happy”)
individual differences in propensities to experience certain social feel­ signals. Perceiving another person’s affective state can elicit various
ings. Measuring stress-related social feelings in the natural environment, feelings in the perceiver (Fig. 11A). First, the perceiver might share the
and beyond momentary time frames, will be helpful for establishing target’s (actual or perceived) feelings (Keysers and Gazzola, 2007;
greater ecological validity for neural correlates. Related to this, because Mayer et al., 2020; Paulus et al., 2013; Waytz et al., 2012). Second,
the second-person neuroscience framework predicts that degree of perceiving another person’s emotional state can lead to feelings of
interpersonal closeness may modulate neural responses (Redcay and confidence in the perceiver if the perceiver is able to accurately decipher
Schilbach, 2019), future research on this topic should involve measuring (and make sense of) the sender’s emotion(s). Third, the perceiver might
this or manipulating it in a laboratory setting (for an innovative perceive the sender’s emotion as appropriate or inappropriate in a given
approach of studying social touch related feelings see (Renvall et al., context (including the perceiver’s own current affective state), leading
2020)). Few studies of stress-related social feelings to date have included to prosocial (e.g., affiliation, compassion) or aversive (e.g., anger,
measures of both peripheral and central neurobiology, making it indignation) feelings. Fourth, if the perceiver views self and the sender

Fig. 11. Brain activity during emotional communication. A) When an individual perceives another person’s emotional behavior, the feelings elicited in the observer
can be characterized as “shared” or “accompanying.” Accompanying feelings include pleasant feelings of confidence if the communication was successful (i.e. the
feeling that one person correctly understood the other person’s feelings), feelings elicited when one partner regards the other partners emotional behavior as
appropriate or not, induction of one’s own emotions regarding the other’s response, and assessing confidence in if the person understands the other’s feelings. B) Use
of pseudo-hyperscanning allows researchers to l examine brain activity of a “sender” and a “perceiver” of emotional signals that can be temporally aligned. When a
person is asked to communicate emotions via facial expressions, their communication partner shows similar neural activation. This is more pronounced between
romantic partners than between strangers. The more similar the activation, the more shared feelings are reported (Anders et al., 2020b). C) Strangers viewing facial
expressions of a sender show an increase in ventral striatum and medial orbitofrontal cortex activity that is correlated with the perceiver’s confidence in having
correctly understood the sender’s emotion and predicts changes in interpersonal attraction (Anders et al., 2016). D) When people were asked to look at images of
another person exhibiting publicly inappropriate behavior (a situation associated with self-reported feelings of Fremdscham or vicarious embarrassment caused by
another’s inappropriate behavior), greater activations in the left insula and anterior cingulate cortex occurred, and decreased activation in the ventral striatum was
observed. In such emerging studies there is no overt communication of feelings or emotions (perceivers inferred the targets’ feeling and emotional states from their
actions in context or not at all), and the degree to which perceivers shared the targets’ feelings are not specifically measured. Future studies, though, may develop
more robust paradigms to address these issues.

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as a social unit (e.g. friends) among more distant others, seeing the fear, respectively, themselves and (ii) neural activity in the ventral
sender displaying emotional behaviors can elicit vicarious feelings in the striatum and medial orbitofrontal cortex (mOFC) (two brain regions that
perceiver (e.g. embarrassment or guilt when a close one behaves play an important role in affiliation, see section 2. Furthermore, neural
emotionally inappropriate towards others) (Müller-Pinzler et al., 2016). activity in the ventral striatum/mOFC and feelings of confidence during
Although all of these feelings might occur in overlapping timeframes, emotional communication were associated with increased feelings of
the perceiver might not be aware of all feelings simultaneously, or might attraction towards the sender after communication (Anders et al., 2016)
experience a blend of feelings rather than a set of distinct feelings. (Fig. 11C). These findings are consistent with the hypothesis that
Neuroscientific studies have been pursued to address the different seamless communication of emotional information can lead to affiliative
types of feelings that can arise during emotional communication to very feelings.
different extents. While numerous neuroimaging studies have focussed Successful emotional communication might not only elicit social
on the mechanisms and processes that might lead to shared feelings in feelings in the perceiver, but also in the sender. In a different study
the perceiver, neuroimaging studies investigating other types feelings participants were asked to submerge themselves into happy or sad sit­
that might occur during emotional communication (we call them uations and to facially express their feelings. At the end of each trial a
“accompanying feelings” hereafter) are very rare. Here we will briefly facial expression was shown that either matched or did not match the
review what is known about the neural processes that might give rise to participant’s facial expression. Facial expressions that matched the af­
shared feelings and accompanying feelings during emotional fective feeling expressed by the participants elicited stronger activity in
communication. the mOFC than facial expressions that did not match the feeling
Early fMRI studies on shared affect compared neural representations expressed by the participant, again irrespective of the emotion that was
of emotions (e.g. disgust) that arise during first-hand experience of that being communicated. Together, these studies suggest a link between
emotion (e.g., smelling an unpleasant odour) to those that arise during neural activity in the ventral striatum/mOFC and positive feelings
observation of the same emotion in another person (e.g., when associated with understanding and being understood during successful
observing another person’s facial expression while they smell an un­ emotional communication.
pleasant odour) in the same individual, bypassing the problem of having As described above, natural face-to-face communication is already
individuals communicating with each other during neuroimaging. While difficult to implement in a neuroimaging environment. This is obtains
in these studies brain regions were identified that are activated during further for face-to-face communication that would be embedded in
first-hand experience and observation of emotion (e.g., the anterior multi-level social contexts able to elicit mixtures of higher order social
insula in the case of disgust, (Wicker et al., 2003)) they neither inves­ feelings. We are not aware of any neuroimaging study that has suc­
tigated communication (i.e., the exchange of information between cessfully accomplished this in a robust scientific manner. With the large
brains) nor did they link neural activity to experiences (feelings). More growth in video face-to-face communications due to the recent
recently, pseudo-hyperscanning has been used to investigate the neural pandemic restrictions of social distancing, investigations of these
basis of shared affective experiences during emotional communication. various platforms may become more timely.
In pseudo-hyperscanning, a “sender” and a “perceiver” are scanned one In an early study, circumvented this problem by linking interindi­
after the other in the same scanner but are connected by audio or video vidual differences in brain activity to trait levels of emotional awareness
recordings such that their brain activity can be temporally aligned after (the ability to recognize and differentiate affective feelings). They found
scanning. In one of these studies (Anders et al., 2011) female partici­ that higher levels of emotional awareness (assessed by the Levels of
pants (senders) were asked to submerge themselves into cued emotional Emotional Awareness Scale, LEAS (Lane et al., 1990)) were associated
situations and to facially communicate their feelings as they arose to with more pronounced local activity in the anterior cingulate cortex
their male romantic partner (perceiver) whom they believed could see (ACC) during emotional experiences. This pointed towards a role for the
them online via a video camera while being scanned in a different ACC in dissociating between different (and possibly conflicting) affec­
scanner. Using classification techniques the flow of affective information tive feelings.
between the sender’s and the perceiver’s brain was examined. This work In a simple approach, Krach and colleagues used contextual stimuli
showed that the senders’ emotion-specific neural activity was reflected (visual sketches of social scenes) in combination with cued imagination
in corresponding neural networks of the perceiver’s brain. Importantly, to study neural processes associated with the self-related feeling of
activity in these networks not only encoded prototypical emotional in­ Fremdscham or vicarious embarrassment (i.e. embarrassment caused by
formation, but information that was specifically related to the sender’s another’s inappropriate behaviour). Scenes associated with Fremds­
specific affective state (Anders et al., 2011). Including more perceivers cham (compared to neutral scenes) elicited activity in the left insula and
(who had not met the senders before) revealed that the sender’s anterior cingulate cortex, and trait empathy correlated with activation
romantic partners simulated the sender’s affective state more accurately parameters in those regions (Krach et al., 2011; Paulus et al., 2015)
in their own brains than strangers (Fig. 11B), and, importantly, that (Fig. 11D). In another study it was shown that neural activity in the
more accurate simulation was associated with a higher degree of shared ventral striatum depended on the perspective participants were asked to
affective feelings (Anders et al., 2020b). This study provided evidence engage. If the task was to imagine another’s inappropriate behaviour
that sharing another person’s affective feelings during emotional and assess one’s vicarious feelings of embarrassment, activity in the
communication might rely on between-brain neural simulation, i.e. the ventral striatum was decreased compared to when participants were
re-enactment of neural processes underlying the sender’s affective state inclined to rate how funny they would find such predicaments (Paulus
in the perceiver’s brain. et al., 2018). However, as in the Lane et al. study, these experimental
A similar study (Anders et al., 2016) revealed that emotional designs did not incorporate overt communication of emotion (perceivers
communication was associated with accompanying feelings of confi­ inferred the targets’ emotion from context or not at all), and the degree
dence in the perceiver if the communication was successful, irrespective to which perceivers shared the targets’ feelings was not measured.
of the emotion that was being communicated. Short videos clips of six Studies investigating the neural processes underlying social feelings
different senders experiencing sadness and fear from the triggered by actions inferred to be emotionally intoned (perhaps indirect
pseudo-hyperscanning study described above were shown to > 90 new or covert forms of emotional communication) may eventually emerge.
participants. The participants’ task was to decide, after each video clip, Thus, neuroscientific studies on social feelings associated with the
which emotion the sender had been experiencing, and to report how communication of emotion are currently heavily constrained by (i) the
confident they felt about their judgement. Self-reported confidence co­ difficulty to elicit complex social feelings in the laboratory, and partic­
varied with (i) the re-activation of local networks in the anterior insula ularly in a neuroimaging environment, (ii) the challenges to measure
that were also activated when the perceivers experienced sadness and complex, dynamically rising, changing and fading feelings in real life,

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and (iii) the lack of analytical techniques and theoretical concepts of 8.2. Social anxiety
how neural and experiential data should be linked once they have been
acquired. While the first problem might be tackled by increased use of Another psychiatric condition where the experience of social feelings
fNIRS (functional near infrared spectroscopy), a technique that suc­ depends on the social domain is social anxiety. Social anxiety is char­
cessfully has been used to measure neural activity of interacting brains acterized by excessive and persistent fears of embarrassment and cor­
(Cui et al., 2012) and that allows measurement of neural activity with responding concerns about others evaluations or criticism. There is
portable devices that can be used over prolonged periods in many evidence that socially anxious individuals have a distorted and nega­
typical social situations (Piper et al., 2014), the second and third tively biased self-image, that, if confronted with an observing and
problems require more conceptual and methodological work (and potentially judging audience, could lead to strong evaluative threats and
interdisciplinary trained neuroscientists with a strong background in to social withdrawal in the long run. Although the social aspect lies at
data analysis techniques). the core of the symptomatology, so far most studies examined social
anxiety in social isolation (Blair et al., 2010, 2011) and showed that the
8. Social feelings in psychiatric conditions processing of fearful faces was associated with increased activations of
the amygdala, ACC, or insula. Only few studies tried to translate the
Social feelings are tightly linked to social interaction and commu­ investigation into real socially interactive scenarios and thereby trigger
nication. Atypical or dysfunctional social communication and interac­ what is at stake in social anxiety.
tion are at the core of various psychiatric conditions, which suggests that One example is a study by Yoshie and colleagues who investigated
social feelings are also affected in individuals with neurodevelopmental the effect of social monitoring on skilled motor performance. In an
disorders or mental health problems. Generally, this can manifest itself interesting fMRI set-up participants were asked to squeeze a pressure
in an altered experience and expression of one’s own social feelings, as sensor to a certain target level within 5 s, displayed in a thermometer
well as in difficulties perceiving social feelings in others. like fashion (Yoshie et al., 2016). After this initial period, participants
were enforced to uphold the same force for another period of 15 s,
8.1. Autism spectrum disorder however now with the thermometer being replaced by a video footage
showing the faces of two experimenters sitting in the MRI control room,
A prominent example of these kind of psychiatric conditions are either with averted gaze (unobserved) or directly observing the partic­
autism spectrum disorders (ASD), which are characterized by persistent ipant (observed). The authors observed a significant increase in the grip
deficits in social communication and social interaction, as well as force in socially anxious participants especially during observation. On
restrictive, repetitive patterns of behavior (American Psychiatric Asso­ the neural level, deactivation of the left inferior parietal cortex predicted
ciation, 2013). A key feature of ASD are difficulties in understanding both inter- and intra-individual differences in socially-induced change in
others’ mental states, especially in situations involving complex social grip force and could show that being observed was linked to enhanced
information (Brewer et al., 2017; Senju, 2013). Although meta-analytic activation within the posterior superior temporal sulcus, a region
evidence suggests a general deficit in emotion processing in ASD, results commonly associated with mentalizing processes (Frith and Frith,
are heterogeneous and it is unclear whether this supposed deficit de­ 2006). A similar modulation of neural activity under social observation
pends on the type of emotion under consideration (Uljarevic and was described above in the study by Müller-Pinzler and colleagues
Hamilton, 2013). Behavioral studies have shown that individuals with (Muller-Pinzler et al., 2015). There, failing in the presence of an audi­
ASD perform equally well to control samples in tasks examining recog­ ence was associated with longer gaze dwell time on social cues and
nition of social emotions such as embarrassment, guilt, or pride (Hillier increased activations of the mentalizing network in socially anxious
and Allinson, 2002; Williams and Happe, 2010). This has been related to participants. Notably, the association of social anxiety and mentalizing
possible compensation strategies that are able to mask emotion recog­ activation was mediated by the dwell time on social cues. In a follow-up
nition difficulties (Williams and Happe, 2010). Neuroimaging studies study by the same group, the authors extended on their earlier findings
could show atypical neural processing of others’ social feelings in in­ by showing that socially anxious participants also exhibited more
dividuals with ASD which could underlie these difficulties. An negatively biased self-related learning, especially when they were
fMRI-study demonstrated that individuals with ASD showed decreased exposed to a judging audience (Muller-Pinzler et al., 2019).
activation in brain areas related to affective sharing, the anterior insula
and ACC, as well as decreased physiological markers of arousal, when 8.3. Schizophrenia and bipolar disorder
confronted with embarrassing scenarios (Krach et al., 2015). Similarly,
another study reported significantly decreased activation in the anterior Although schizophrenia and bipolar disorder are both associated
insula and posterior superior temporal sulcus in individuals with ASD with emotion processing deficits, Tabak et al. (2015) identified that
when inferring others’ social emotions (Aoki et al., 2014). measures of feeling states in these conditions were strongly related to
Few studies have also focused on the experience and expression of daily functioning. Specifically, a clarity of feelings subscale in the
social feelings in ASD. For instance, one study showed that children with schizophrenia sample was significantly correlated with independent
ASD, compared to typically developing children, were less likely to living ability. In the bipolar disorder sample, higher attention to their
report reasons for their feelings, specifically self-conscious emotions like subjective feelings was significantly associated with better social func­
guilt and shame, and provided more script-like accounts of emotional tioning. Ospina et al. (2019) took the approach of investigating alex­
experiences (Losh and Capps, 2006). However, this could not be shown ithymia in similar patient samples. Alexithymia refers to difficulty
in adults with ASD (Williams and Happe, 2010). Also, the majority of recognizing and describing emotional experiences of the self. It can
research in ASD is based on the study of individuals without intellectual include symptoms such as impairment in identifying and describing
disability. This is even more evident for the study of social feelings in feelings as well as distinguishing feelings from bodily sensations. Results
individuals with intellectual disabilities that is almost entirely neglec­ indicated that both schizophrenia and bipolar samples were signifi­
ted. One of the few studies in this field targeted “social” abilities un­ cantly impaired on an alexithymia scale sensitive to describing and
derlying observational learning and correlated performance measures identifying feelings, which was predictive of social functioning in the
with cortical thickness (Foti et al., 2018). So far, there is no study bipolar disorder sample. Interestingly, neuroanatomical correlates to
addressing the neurofunctional level of social interaction and related alexithymia symptoms include the medial prefrontal cortex and anterior
feeling states in ASD with intellectual disabilities. cingulate (both component structures of the social brain network) in
bipolar disorder as well as control samples. These results align well with
the broader model recently proposed by Porcelli et al. (2019) that

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identified social withdrawal as a core, underlying deficit in diverse occipital/fusiform cortex, temporo-occipital cortex, and para­
conditions in which social dysfunction comprises a dominant disability hippocampal gyrus.
including schizophrenia, major depression and Alzheimer’s disease. As In addition to social media, social feelings are also being studied as
part of this impairment, we hypothesize that social withdrawal results part of the attraction to reality TV programs (Lewis and Weaver, 2015).
from emotional detachment, lack of emotional engagement (i.e., lack of For example, observing violations of social norms or others embarrass­
“knowing others” through emotional engagement and interaction) and ing themselves activated brain regions associated with theory of mind,
attenuated social feelings (experiencing and responding to). empathy, and social identity (Melchers et al., 2015).

9. Social media 10. Extracting neural networks related to social feelings with
quantitative meta-analyses
The growth of social media appears to be fueled by natural and
strong social motives and drives. These novel platforms continue to We conducted meta-analyses across imaging studies from the liter­
proliferate and evolve with increasingly mobile and easily accessible ature with Neurosynth (http://www.neurosynth.org; Yarkoni et al.,
technology to the point where 2 billion users around the globe partici­ 2011) to quantitatively extract the neural networks of mental processes
pate in hundreds of types of social networks. Important generational relevant for social feelings as discussed in the review. Neurosynth is a
differences may exist that have implications for social-emotional func­ platform for large-scale, automated synthesis of fMRI data including
tioning and neurocognitive architecture based on exposure during sen­ 507,891 activations from 14,371 studies (30th April 2020). As an
sitive developmental periods (Crone and Konijn, 2018). For example, automated brain-mapping framework Neurosynth applies text-mining
contemporary American adolescents are estimated to be involved in 6− 9 and meta-analysis techniques to generate a large database of map­
hours of social media on a daily basis (excluding home- and schoolwork) pings between neural and cognitive states.
(Rideout, 2015). Activation coordinates and frequently terms are automatically
From a neuroscience perspective, many important questions quickly extracted from published neuroimaging articles. The entire database of
arise such as the neural substrate that supports and rewards such social coordinates is divided into two sets for each term of interest, these that
media behaviors, and how similar and different it is from typical, direct are reported in articles containing the term, and those that are reported
social action/interaction. The ease of access, variety of social media in articles not containing the term. Thereafter, the meta-analysis com­
platforms, and constantly changing trends and topics may provide fertile pares the coordinates reported for studies with and without the term of
opportunities for activation of the seeking system (Panksepp and Biven, interest. Images are corrected for multiple comparisons with a false
2012). In this review, our focus is on discussing what is currently known discovery rate (FDR) of 0.01. We included only positive results and
about social feelings in relation to social media behaviors its neural report results for the association test regarded as more reliable than
correlates. results for the uniformity test. Here, the association test map reports z-
From a theoretical perspective social media would appear to share a scores from a two-way ANOVA testing for the presence of a non-zero
good deal of overlap with processes of social cognition (such as men­ association between the term used and voxel activation, whereas the
talizing, theory of mind, empathy), social emotions (e.g., awe, contempt, uniformity test map shows z-scores from a one-way ANOVA testing
gratitude, embarrassment) and social feelings (e.g., trepidation, affilia­ whether the proportion of studies that report activation at a given voxel
tion, disgust). Digital resources have even devised attempts to provide differs from the rate that would be expected if activations were uni­
some forms of visual signals (e.g., emoticons) to enhance transmission formly distributed throughout the gray matter. Consequently, the as­
and perception of salient emotional and feeling states to mimic natural sociation test maps allow making more confident claims that a given
appearances. Why go through all these efforts? The opportunities to region is involved in a particular process, and is not only involved in
connect with more people in quick, efficient ways that one can control almost every task (corresponding approximately to “reverse” and “for­
(and potentially portray and modify impressions, opinions, and influ­ ward inference” maps; for details see http://www.neurosynth.org).
ence) can bring rewards (Tamir and Mitchell, 2012). These can take the Eventually, association test maps show whether activation in a region
forms of ‘Likes’ and other feedback that may be highly motivating occurs more consistently for studies that mention the current term than
(Meshi et al., 2013). for studies that do not mention it. Resulting maps were downloaded and
Meshi et al. (2015) identified 5 key social media behaviors: broad­ visualized with MRIcron (http://www.mricro.com; version 1st June
casting information, receiving feedback on information, observing the 2015). For methods applied, please refer also to two other papers using
broadcasts of others, providing feedback on the broadcasts of others, and the same approach in this volume (Frewen et al., 2020; Stefanova et al.,
comparing oneself with others. Considering what is known about the 2020).
social brain network, they argued that mentalizing was likely to be Meta-analyses were conducted for the terms affective (748 studies
invoked by several of these behaviors, along with self-referential as well identified; 28,542 activations reported), emotional (1708; 58,326),
as self-other processing. These have been linked to the social brain empathy (187; 7913), feelings (149; 5414), moral (87; 2806), social
network regions including the dorsomedial and mPFC, superior tem­ cognition (220; 8247), social interactions (123; 4900), stress (321;
poral sulcus, temporoparietal junction, anterior temporal lobe, and 8294), and theory mind (181; 7761).
posterior cingulate/precuneus. The quality of individual extracted studies in the database may be
The motivating force of social media was supported by fMRI data low, because of the automated uncontrolled process. Here, quality
generated from a sample of healthy adolescents and young adults. These means controlling for strict fulfilment of inclusion and exclusion criteria
individuals provided ‘Likes’ to posted pictures and experimentally (for further discussion see last paragraph of this chapter). Moreover, not
received ‘Likes’ to pictures they posted in a simulated social media all journals are covered and terms covered in the database are limited.
posting paradigm. Providing ‘Likes’ to posted pictures was associated Hence, results represent an orientation to be proved by other better
with activations in the ventral striatum and ventromedial prefrontal controlled meta-analytic approaches. To adjust for this bias, at least
cortex as well as the dorsal striatum and portions of the thalamus, limbic partly, we considered only terms that were based on at least 100 studies.
system and frontal-parietal cortices (Sherman et al., 2018). In contrast, Only for moral the number of studies was below that threshold. More­
when receiving feedback of ‘Likes’ on posted photos, activations were over, we chose the term with the maximum number of studies if terms
detected in the dorsal and ventral striatum, thalamus, brain stem/VTA, covered related concepts, i.e. affective (not affect), emotional (not
frontal lobe, occipital lobe and cerebellum. Conjunction analysis emotion), feelings (not feeling), social interactions (not social interac­
revealed 2 large clusters: (1) bilateral ventral and dorsal striatum, tion) and theory mind (not mentalizing). Furthermore, we applied a
thalamus, hippocampus, brain stem and VTA; and (2) left lateral strict FDR of 0.01 and reported only results for the association test

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regarded as more reliable than the uniformity test. Finally, we con­ meta-analyses showing significant findings there. Results are illustrated
ducted conjunction analyses to further strengthen the validity of our in the right part of Fig. 12, and in related movies in the supplementary
findings. These analyses correspond to overlap analyses for significant material. This conjunction analysis confirmed for “hot” social functions,
function-associated regions (for more detailed explanation see below). as shown in orange color, the frontomedian cortex and ACC, subcallosal
As illustrated in Table 1 and the left part of Fig. 12 networks included area, OFC, insula, and amygdala as the most consistent hubs in this
frontomedian cortex and ACC, subcallosal area, frontolateral cortex and neural network. The conjunction analysis for “cold” social functions as
OFC, temporo-parietal junction, temporal pole, precuneus, insula, shown in blue color identified the frontomedian cortex and ACC, sub­
amygdala, midbrain and pituitary gland. The globus pallidus and callosal area, frontolateral cortex and OFC, temporo-parietal junction,
mammillary bodies were only identified in one mental function, temporal pole and precuneus as the associated network. Finally, we
respectively. Obviously, there was a separation in rather “hot” or conducted a meta-analysis across all social functions, i.e. including both,
emotional-affective social functions, i.e. the neural correlates of the “cold” and “hot” social functions (spectrum colors), which revealed as
terms affective, emotional, feelings, stress, and empathy, and the neural relevant networks the frontomedian cortex and ACC, subcallosal area,
correlates of “cold” cognitive social functions such as moral, social frontolateral cortex and OFC, temporo-parietal junction, temporal pole,
cognition, social interactions and theory of mind. Table 1 illustrates both precuneus, insula, amygdala and midbrain. In sum, the conjunction
concepts and their neural correlates in orange (“hot”) and blue color analysis confirmed findings of the single meta-analyses shown in
(“cold” functions). Note that some regions, as illustrated in light color, Table 1.
could intermediate between “hot” and “cold” social functions, i.e. the As already mentioned, Neurosynth has limitations regarding the
temporal pole and precuneus as well as the amygdala and midbrain. quality of individual extracted studies, because of the automated un­
Related social functions are feelings, empathy, social cognition and so­ controlled process to extract activation coordinates and frequently used
cial interactions with intermediate nature between “cold” and “hot” terms from papers, and because it covers a limited number of journals
social functions. Moreover, frontomedian cortex and ACC, subcallosal and terms. Hence, results shall be proved by other better controlled
area, OFC, and insula were relevant for both, “hot” and “cold” social meta-analytic approaches. Then, study selection shall be based on sys­
functions. Remarkably, the pituitary gland, involved in secretion of tematic screening in databases like PubMed / Medline and by applying
socially-acting hormones such as OT and vasopressin, was also high­ strict inclusion and exclusion criteria, where study’s suitability is
lighted by three functions, i.e. stress, empathy and social interactions. checked by two independent reviewers (see preferred reporting items
Moreover, we conducted a conjunction analysis across the neural for systematic reviews and meta-analyses – PRISMA – guidelines (Moher
networks of all investigated mental functions to extract brain regions et al., 2009). One might also cross-validate findings by using other
that reached significance with the chosen threshold (FDR corrected) quantitative techniques such as activation likelihood estimation (ALE)
criterion of 0.01 for more than one function. This conjunction illustrates or seed-based d mapping (SDM; formerly coined signed differential
regions, where results for single meta-analyses overlap, i.e. several mapping) meta-analyses, or conducting analyses in the better controlled

Table 1
Neural networks related to social feelings and related mental functions as revealed by the Neurosynth database.1

1
Dark colors illustrate regions where more than one-half of “hot” or “cold” social functions showed activations. Light colors illustrate regions that were intermediate
between “hot” and “cool” social functions, i.e. temporal pole and precuneus as well as amygdala and midbrain. Note that the frontomedian cortex and anterior
cingulate cortex, subcallosal area, orbitofrontal cortex, and insula were relevant for both “hot” and “cool” social functions.

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Fig. 12. Neural networks of mental functions related to social feelings as revealed by the Neurosynth database. Left: Maps extract regions, marked in red, where
activation occurs more consistently for studies that mention the term than for studies that do not. Right: Conjunction analysis indicating regions where neural
networks overlap for two or more mental functions. Results are shown separately for the five “hot” and four “cold” mental functions (orange or blue color,
respectively), and for all nine mental functions together (spectrum colors). Number of regionally overlapping functions is color coded as shown on respective scale.
ACC anterior cingulate cortex, FMC frontomedian cortex, L left, OFC orbitofrontal cortex, PC precuneus, R right, SA subcallosal area, TP temporal pole, TPJ tem­
poroparietal junction. Results for conjunction analyses are additionally illustrated in respective movies in the Supplement.

Brainmap database (Albrecht et al., 2019a, b; Schroeter et al., 2020, “Social“, which was defined as follows:
2014). We checked systematically whether studies compared directly
Feelings related to the way a person interacts with others (e.g.
Neurosynth with other meta-analytical approaches, such as ALE or SDM
accepting, ungrateful, etc.). feelings related to the way others
(systematic search in PubMed on 1st July 2020: keywords (i) neurosynth
interact with that person (e.g. appreciated, exploited, trusted, etc.),
activation likelihood estimate meta-analysis, (ii) neurosynth signed
or feelings of one person for or towards others (e.g. sympathy, pity,
differential mapping meta-analysis, (iii) neurosynth seed-based d map­
etc.) that are not covered by other categories (specifically, does not
ping meta-analysis). Although a systematic comparison is missing and a
include feelings of Anger, Fear, Attraction or Repulsion).
desideratum for the future, two studies using both techniques, Neuro­
synth and ALE, demonstrated consistent findings (Andrzejewski et al., This subset of the results included about 637 feeling word senses (see
2019; Parro et al., 2018). Moreover, smaller brain structures such as the Supplemental data accompanying this review). It was not within the
septum might not be detected in imaging-based meta-analyses due to scope of this effort to undertake a formal analysis of this dataset, but we
limited spatial resolution of these methods. While keeping these con­ reviewed these feelings words and attempted to roughly organize the
straints in mind, we regard the meta-analytical findings as relevant to words into discernable categories. Initial steps were undertaken to
the neurobiology of social feelings. identify and classify such a semantic class and differentiate it from other
feeling word classes. We identified eight major social domains where
11. Linguistics feelings could be categorized. These included: (1) social communica­
tions, (2) own behaviour, (3) reaction to others, (4) reaction of others,
To better understand the range of verbally articulated feelings that (5) social affiliation, (6) social power, (7) treatment of others, and (8)
are expressed in the English language, a task team within the Human treatment by others.
Affectome Project led a computational linguistics research effort to These domains can be applied to agents, recipients, and interaction
identify feeling words (Siddharthan et al., 2018). Results were extracted contexts. Subcategories were further identified for more specific feelings
from the Google n-gram corpus (which includes roughly 8 million books associated with disapproval, trusted, betrayal, compassion, friendly,
(N and Reips, 2019) and then manually annotated by more than one loving, dominant etc. Positive and negative interactions, by intention
hundred researchers from this project. This resulted in 9 proposed cat­ and by outcome, constitute additional axes.
egories of feelings and a new affective dataset that identifies 3664 word Caution should be exercised in the interpretation of this list since it
senses as feelings. Of relevance to this review is a category related to

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was created only to provide an initial sense of how feeling words related observations suggest several hypotheses regarding the alerting,
to one another. Although these remain far from a validated set of stimuli arousing, saliency and adaptive value of social stimuli and social expe­
and identifiable categories for experimental application, developing a rience on environmental monitoring, allocation of attentional resources,
standardized set of ‘social feeling words’ may have a place in stimulating and the affective/reward value of such processing. Within those com­
research on the underlying parameters of social feelings.Thus, we have putations, feelings associated with integrated forms of attention and
included this dataset in the supplemental materials. In our opinion, the social processing can be examined and tested.
list warrants more in depth exploration and may deepen our under­
standing of the feelings in this domain. 12.3. Hedonics
Other approaches to further linguistic analysis can consider neuro­
linguistics. For example, ‘wronged’ as a social feeling word appears Feelings of pleasure from engagement within certain social contexts
related to the specific action of another. There is a similar sense to have been thought to provide reinforcing and rewarding associations,
feeling ‘ostracized’, ‘bruised, and insulted’ which all can result from the though such mechanisms remain largely unknown. Touch has been
specific words and actions of others. In contrast, ‘gratitude’, ‘compas­ associated with a variety of reported hedonic feelings (e.g., pleasure,
sion’, and ‘malice’ are descriptive state terms that refer to attitudes and pain, disgust, and comfort) and linked to both the endogenous opioid
behavioral characteristics. Studies in patients with cerebral lesions have system and oxytocin mediation among others (Nummenmaa et al.,
demonstrated that the neural mediation of actions words (i.e., verbs) is 2016). Both context and motivation for touch appear to have substantive
quite different from nouns. Correlation to lesion sites indicated that influences on the social aspects of the hedonic feelings that are begin­
deficits in generating such words are associated with the inferior frontal ning to be delineated (e.g., Ellingsen et al., 2015). In an intriguing
lobe and temporal lobe, respectively (Piras and Marangolo, 2007). These experiment, Manninen et al. (2017) investigated whether social
findings raise the possibility that the semantic representation of certain laughter, as an example of larger group social bonding activity, might
social feelings may be distributed in a neural network that varies with activate the μ-opioid-receptor in a similar way as touch and grooming
the properties of what gives rise to the feelings, e.g., the specific actions have been linked to endogenous opioid production. Results revealed
of another on the perceiver vs. encountering another’s behavioral that laughter was associated with endogenous opioid release in several
characteristics indirectly, by differing valence, and in-group/out-group brain regions linked to reward and arousal (thalamus, caudate nucleus),
effects, among others. with baseline endogenous opioids levels predictive of social laughter
and detectable in structures such as the amygdala, ventral striatum, and
12. Interactions and directions frontal and cingulate cortices. In contrast, experimental paradigms that
manipulated social inclusion/exclusion identified limbic system acti­
There are several areas of important interactions with other Human vations associated with distress and feelings of rejection. Recurrence of
Affectome team inquiries within this special issue that relate to social distress and associated limbic system activation were also detected with
feelings. These are highlighted briefly below. reminiscence about past interpersonal stressors.
Areas of promising research pertinent to social feelings are emerging
12.1. Anger across the lifespan spectrum as well.

Anger is associated with diverse feelings that are directed towards 12.4. Parental neuroscience
another (or others) based on their actions that are perceived as unfair
and/or disruptive to one’s plans, goals and expectations. Anger has been The study of the parental brain requires a combination of well-
considered to be a basic and a social emotion. Hence, there typically are established paradigms and innovative, realistic probes that incorpo­
suspected strong neurobiological foundations linked to personal well- rate consistent terminology on affect. More naturalistic and personally
being and adaptation but also social expectations, coordination and relevant stimuli must be pursued to carefully assess real-time parental
removal of social obstacles (Williams, 2017). Untoward reactions may brain functioning, thoughts and behaviors (Kim et al., 2013) to include
take the form of hostility and aggression towards others (e.g., Klimecki the richness of parental feelings and real-time nature of parent-infant
et al., 2018). Such reactions may be mediated in part by specific social interactions (Safyer et al., 2020). For example, brain activity in
factors such a power status that may sway feelings regarding potential response to own baby-cry was correlated with a measure of mental state
actions and consequences (Li et al., 2016). The social contexts of anger talk, but not with more global aspects of observed caregiving (Hipwell
and the mediating role of feelings associated with power status, other et al., 2015). Current literature suggests mixed evidence for anatomical
types of relationship and other social factors leads to new hypotheses and functional correlations. Thus far, one human study suggests struc­
regarding the role, intensity and resolution of anger behaviors. Regu­ tural changes occur in the maternal brain over the early postpartum,
lation of angry feelings may play an important mediating role in many including correlations with positive perception of baby (Kim et al.,
forms of social interaction and decision-making (Gilam et al., 2015). The 2010) – a construct well connected with feelings.
factors and variables contributing to individual differences in this area High-stress environments such as poverty, being a single or teenage
require further investigation. parent, high marital conflict, and substance exposure are significant risk
factors for maternal insensitivity toward infants (Magnuson and Dun­
12.2. Attention can, 2002; Roubinov and Boyce, 2017; Sripada et al., 2014; Sturge-Ap­
ple et al., 2006). This calls for more specific studies from brain imaging
There appear to be strong interactions between attentional and social perspectives to determine specific mechanisms. Such specificity, as well
brain mechanisms that are beginning to be identified and characterized. as more work on healthy parents, will be critical for developing targeted
For example, social stimuli can attract first saccades more frequently interventions and treatments that are effective to prevent psychopa­
along with a larger portion of visual attention to scenes (Rosler et al., thology for those at risk, improve symptoms of psychopathology among
2017). Direct gaze can act as a type of prime for socially-relevant ac­ parents already affected and cross generations to improve offspring
tions, particularly when combined with precise body movements that mental health.
engage interaction (Betti et al., 2018). Furthermore, viewing patterns of
social stimuli (for own species and cross-species) were discovered to be 12.5. Social isolation and loneliness
individual and species-specific in human and nonhuman primates, and
possibly based on natural characteristics as well as experiential factors Being socially distanced or socially isolated negatively affects health
that develop through adaptation (Kano et al., 2018). These initial and mortality risk (Pantell et al., 2013; Singer, 2018). This may be

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related in part to a change in social feelings. These effects have been a important roles in social experiences and appear to signal underlying
special concern for elderly living either in retirement communities and mechanisms that influence and modulate behavior. Feelings in general
nursing homes or alone at home More recently, the relevance and po­ are geared toward aiding homeostasis, adaptation and well-being. Social
tential toll of social isolation has been highlighted for persons of all ages feelings are particularly germane to navigating, adapting and thriving
by events associated with the coronavirus pandemic in 2020. In addition within a complex and changing social world, which is a major facet of
to objective social isolation, however, feelings of loneliness have been contemporary life. The spectrum of the social world is quite broad,
associated as well with poorer physical health (Cacioppo et al., 2014) ranging from the most intimate types of relationships to common home,
and with elevated risk for premature mortality (Holt-Lunstad et al., community, educational or occupational settings and even larger soci­
2017). Dementia is also an increasing scourge in aging societies (Fox and etal concerns that each require managing spontaneous social in­
Petersen, 2013). The combination of coronavirus restrictions and de­ teractions and a social self.
mentia can be considered as a “double hit” for many patients and their We defined social feelings as subjective experiences that arise in
families, as loneliness, social withdrawal and isolation are already interaction with others or when being remembered and when recalling
concerns for patients with dementia (Wang et al., 2020). Even in the others’ behaviors, thoughts, intentions or emotions. As such, social
digitally-experienced younger generations, the effects of sustained social feelings have been invoked in studies of emotional contagion,
distancing on physical and mental health may be evoking odd and un­ attachment, affiliation, empathy, influence and well-being as well as
usual social feelings. Digital social networks clearly are not the same as disorders of such processes. There remain a variety of challenges to
interacting in person, but the shared experiences of social distancing address, including the role of the mirror neuron system, identifying in
may prove beneficial to certain innovations in occupational, educa­ what ways social feelings are influencers on others, how social feelings
tional, health care delivery and other interpersonal activities. Studies of mediate belongingness as well as loneliness, and the mechanisms of
recent unprecedented social isolation and its varied consequences de­ extended attachments beyond kinship that are based on shared social
serves more specific attention from the perspective of social feelings. feelings. It is particularly important to investigate how these processes
modify decision-making, adjustment and computational neuroscience
12.6. Interpersonal trauma models.
Feelings are beginning to be considered in social neuroscience
With respect to social feelings and interpersonal stress, an important research and models as key component processes. They are being
future direction is to extend this research to persons exposed to inter­ identified as contributors to mother-infant attachments and more
personal trauma. Trauma-related disorders have traditionally been broadly to parenting behaviors, moral sentiments, interpersonal stress
conceptualized as fear or anxiety-related disorders. However, exposure including social evaluative stress, social exclusion, interpersonal trans­
to interpersonal trauma, and especially trauma that occurs in close re­ gressions, and emotional communications. There is increasing interest in
lationships, is also associated with social feelings such as betrayal, understanding the social feelings dimension of psychiatric disorders (e.
shame and humiliation during the immediate aftermath of the event g., autism spectrum, social anxiety, schizophrenia, bipolar disorder),
(Kaysen et al., 2005), as persons reflect back on their experience and the underlying dysregulation that affects social adaptation. Animal
(Amstadter and Vernon, 2008), and in response to subsequent social model research has been most prominent in identifying important
threat (Platt and Freyd, 2015). Moreover, these social feelings may help neurotransmitter and neurohormonal modulators involving key struc­
explain the more severe mental health symptoms reported by persons tures within the social behavior neural network. Throughout the
exposed to interpersonal versus non-interpersonal trauma (Badour et al., neuroscience literature reviewed, there is increasing evidence that social
2017; La Bash and Papa, 2014), and the severity of specific symptom feelings are mediated, at least in part, by structures associated with the
clusters such as avoidance and emotional numbing (Kelley et al., 2012). social brain network. There appears to be extension, though, to a
Studies of the neurobiology of these social feelings may further identify broader network of structures throughout the paralimbic (e.g., sub­
mechanisms of illness in interpersonal trauma, and targets for genual, insula), limbic (e.g., septum, amygdala) and midbrain regions
intervention. that likely mediate important effector mechanisms for mental and
embodied experiences of socially-relevant feelings. These proposed as­
12.7. Social sensitivity feelings sociations were confirmed by the meta-analysis of brain regions
involved in social feelings which utilized the Neurosynth platform for a
A curious defect in social feelings may be hallmark of certain in­ large-scale, automated synthesis of functional magnetic resonance im­
dividuals identified as psychopathic. Such individuals may be described aging (fMRI) data. Converging methods of structural and functional
as callous, unfeeling, cold, and taking pleasure from the pain of others. neural network analyses will be needed to confirm these initial obser­
Despite the apparent lack of social feeling for other’s pain and well- vations. Intriguing avenues of emerging research concerns the evolving
being, such individuals may nonetheless display preserved moral social media landscape, pandemic mandated video-education experi­
reasoning and knowledge, at least upon formal questioning (e.g., know ences, and work-from-home occupational modifications many people
right from wrong by cultural standards). Yet, such knowledge does not have experienced.
drive or regulate their actions. Hence, an identifiable cognitive deficit Increasingly powerful experimental and neuroimaging methods are
has not been consistently identified in these cases, with some hypotheses being combined with meaningful and nuanced assessment of the feelings
positing that the defect emanates from a fundamental emotional, of social life in order to provide a more comprehensive account of what
empathic and/or social feeling deficit (e.g., Cima et al., 2010). This in drives, regulates and maintains adaptive and healthy social behavior.
turn prevents experiencing a sense of guilt, embarrassment or shared This will require an integration not only with neuroanatomical and
pain that one might expect from intentional violent harm perpetrated on neurophysiological mechanisms but also constructs of cognition and
others. The neurobiological and psychological bases for a ‘feeling defect’ emotion in order to delineate both typical, adaptive processes and
requires further investigation. various pathological forms of social feelings. Towards that end, we have
identified relationships that exist between social feelings and other areas
13. Conclusions of affective research within the special issue “Towards an Integrated
Understanding of the Human Affectome” (i.e., Physiological, the Self,
In this review, we considered social feelings from a neuroscience Anticipatory, Actions, Attention, Motivation, Anger, Fear, Happiness,
perspective and propose that the notion of social feelings represents Sadness, and Hedonics), summarizing future research needs in this
natural kinds of neurobiological processes that can be distinguished burgeoning domain.
from emotion and are conducive to scientific inquiry. Feelings play

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P.J. Eslinger et al. Neuroscience and Biobehavioral Reviews 128 (2021) 592–620

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Atzil, S., Hendler, T., Feldman, R., 2014. The brain basis of social synchrony. Soc. Cogn.
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