REVIEW

published: 19 April 2018

doi: 10.3389/fpsyg.2018.00575

Psychopathy to Altruism:
Neurobiology of the Selfish–Selfless
Spectrum
James W. H. Sonne 1* and Don M. Gash 2
1
Department of Health Professions, University of Central Florida, Orlando, FL, United States, 2 Department of Neuroscience,
University of Kentucky, Lexington, KY, United States

The age-old philosophical, biological, and social debate over the basic nature of
humans as being “universally selfish” or “universally good” continues today highlighting
sharply divergent views of natural social order. Here we analyze advances in biology,
genetics and neuroscience increasing our understanding of the evolution, features
and neurocircuitry of the human brain underlying behavior in the selfish–selfless
spectrum. First, we examine evolutionary pressures for selection of altruistic traits
in species with protracted periods of dependence on parents and communities for
subsistence and acquisition of learned behaviors. Evidence supporting the concept
Edited by: that altruistic potential is a common feature in human populations is developed.
Roumen Kirov,
Institute of Neurobiology (BAS), To go into greater depth in assessing critical features of the social brain, the two
Bulgaria extremes of selfish–selfless behavior, callous unemotional psychopaths and zealous
Reviewed by: altruists who take extreme measures to help others, are compared on behavioral traits,
Sue Llewellyn,
structural/functional neural features, and the relative contributions of genetic inheritance
The University of Manchester,
United Kingdom versus acquired cognitive learning to their mindsets. Evidence from population groups
Livia Colle, ranging from newborns, adopted children, incarcerated juveniles, twins and mindfulness
Università degli Studi di Torino, Italy
meditators point to the important role of neuroplasticity and the dopaminergic reward
*Correspondence:
James W. H. Sonne systems in forming and reforming neural circuitry in response to personal experience
james.sonne@ucf.edu and cultural influences in determining behavior in the selfish–selfless spectrum. The
underlying neural circuitry differs between psychopaths and altruists with emotional
Specialty section:
This article was submitted to processing being profoundly muted in psychopaths and significantly enhanced in
Psychopathology, altruists. But both groups are characterized by the reward system of the brain shaping
a section of the journal
Frontiers in Psychology
behavior. Instead of rigid assignment of human nature as being “universally selfish” or
Received: 04 January 2018
“universally good,” both characterizations are partial truths based on the segments of
Accepted: 05 April 2018 the selfish–selfless spectrum being examined. In addition, individuals and populations
Published: 19 April 2018 can shift in the behavioral spectrum in response to cognitive therapy and social and
Citation: cultural experience, and approaches such as mindfulness training for introspection and
Sonne JWH and Gash DM (2018)
Psychopathy to Altruism: reward-activating compassion are entering the mainstream of clinical care for managing
Neurobiology of the Selfish–Selfless pain, depression, and stress.
Spectrum. Front. Psychol. 9:575.
doi: 10.3389/fpsyg.2018.00575 Keywords: heredity, social, cultural, genetic, neural circuitry, emotions, empathy, compassion

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

INTRODUCTION levels of empathy and compassion that strongly influence their

worldview and role in society.
In the mid-1800s, the French Philosopher Auguste Comte
constructed the word altruism from the Latin alteri (“others”)
to name his vision of a moral call to place the needs EVOLUTION OF THE PROSOCIAL BRAIN
of others over one’s self-interests. Altruism has since been
defined in many senses, including an extreme selflessness in The term “altruism” has meant many different things in different
undertaking actions benefiting others without evident self- times and places. Since Comte’s moral call to place the needs of
benefit and incurring personal risk. The conundrum created by others above one’s own needs, different disciplines have applied
Comte’s concept continues to reverberate through social debate, different definitions, and the semantics are themselves a necessary
philosophy, theology, and biology, highlighting complex issues starting point (West et al., 2007). Group selection theory explains
in the spectrum of behavior ranging from extreme selfishness to behavior such as kin sacrifice in terms of gene survival as
extreme selflessness (Ricard, 2015). The very concept of altruism opposed to individual survival (Simon et al., 2013; Gardner,
raises important issues underlying two sharply divergent views of 2015). Therefore, according to this evolutionary theory, related
natural social order. individuals will be more likely to perform altruistic acts and
Philosophical, political and biological arguments on whether decrease their own survival if it benefits the survival of a related
humans are naturally selfish or unselfish have flared for individual that carries many of the same genes. This theory is
centuries and continue today. Thomas Hobbes contending in his supported by extensive evidence in the literature of preferential
work Leviathan printed in 1651 supporting strong Monarchist treatment of kin (Madsen et al., 2007), while others argue that
governments and running through current culture in Ayn Rand’s group selection is an emergent property of natural selection by
popular works assert there is a natural “universal selfishness” individual fitness (Zhang et al., 2014; Kennedy et al., 2018). One
manifest in humans, with all behaviors characterized as altruistic question is how kin-preference is identified and conferred by an
being in reality actions that in some measure were in the organism. Kin-preference may be a function of the extensive time
actor’s best interest. Rand’s continuing influence on political spent with and proximity to the relative as opposed to an ability
discourse can be seen in the powerful American Speaker of to identify genetic relatedness, as argued by cases of cronyism
the House and former Vice Presidential candidate Paul Ryan’s and altruistic preference for close friendships (Stewart-Williams,
attribution of Rand’s Atlas Shrugged as formative in developing 2008). From an evolutionary biology perspective, “altruism” or
his political principles (Weiner, 2012). In Biology, the Oxford empathic acts could be selected for culturally as a sign of fitness
University Lecturer and popular science author Richard Dawkins (Taborsky et al., 2016), as attested to by examples of prosocial
has proclaimed, “We are survival machines – robot vehicles behavior for non-relatives across the animal kingdom (Field and
blindly programmed to preserve the selfish molecules known as Leadbeater, 2016; Wilkinson et al., 2016). A more semantically
genes” (Dawkins, 1976). “true” form of altruism may have its roots in the parental instinct
Sharply alternate opinions more supportive of Comte’s vision to care for offspring, and may explain why empathic behavior
have also resonated for centuries and continue unabated. Two is more commonly observed in species with protracted periods
highly influential 18th century philosophers David Hume and of pre-adult growth (Preston, 2013) requiring extended rearing
Jean Jacques Rousseau argued that by nature humankind is and the resultant passing of learned behaviors, called acquired
unselfish. A contention strongly supported today by the prolific cognitive learning, as well as “neuron-based heredity,” including
neuroscientist and popular science author Richard Davidson social and cultural factors that may have genetic and cognitive
(Davidson, 2015). A middle position emphasizing a dual nature elements (Gash and Deane, 2015), to come into play. Thus, the
for humankind was presented in the 15th century essay by Pico importance of passing to kin the learned behaviors promoting
della Mirandola Oration on the Dignity of Man, asserting that we culturally selected traits of compassion may counterbalance the
can shape our own destiny by freely choosing whether to descend selective value of genes promoting extreme selfish behavior (Bell
into brutish behavior or rise to the superior orders of the divine. et al., 2009).
This is a vision expanded upon by the Dalai Lama who wrote The concept of altruism as an enhanced parental instinct relies
that “the most important thing in this existence of ours is to do on the evolution of several factors in both the altruist and the
something that can be of benefit to others. What we need more recipient: signaling of kinship status and need for compassion,
than anything is to develop an attitude of altruism – that is really recognition by kin of the signals, and donation-behavior by
what gives meaning to life” (Dalai Lama, 2007). the kin (Sinervo et al., 2006). While this behavioral signaling
The second debate invariably accompanying any discourse mechanism may underlie parental instinct and compassion
on altruistic behavior is what is due to nature versus nurture. which is probabilistically directed toward kin, it is possible that
To better understand the scientific basis for addressing such simple parental behaviors – such as offspring retrieval, sustenance
profound social and philosophical issues, here we examine the and shelter sharing, and emotional comforting – are behavior
biology and neurological basis of human altruism. We analyze the patterns of signaling-recognition-action that have been enhanced
neural systems and the role of heredity, both genetic and neuron- by evolutionary mechanisms (Preston, 2013) resulting in broader
based (cultural and social), in the development of behavior in the altruistic behavior from prosocial brains with greater capacity for
selfish–selfless spectrum, with the goal of discovering how and receiving and passing on experience and acquired information.
why portions of the population experience dramatically differing And as recent studies have shown, parenting-associated prosocial

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

helping behaviors not only enhance the survival of the offspring,

but also promotes better health, slower decline in functioning
levels and lower risk of mortality for care-givers (Brown and
Brown, 2015). Collectively, the evidence indicating prosocial
altruistic capability provides for complex interactions that have
come to form the foundation of our civil, societal interactions
(Matusall, 2013). Social interactions often extend not only to
members of our families, but to other members of our own social
species, and often to members of other domesticated species on
which we depend for our survival and social well-being.

THE SELFISH–SELFLESS SPECTRUM

Human evolution, especially since the separation from the last
common ancestor shared with the great apes, is posited to have
been driven by bipartite hereditary processes involving genetic
and neuron-based systems (social and cultural heredity) (Gash
and Deane, 2015). The development of large interactive social
groups that share resources and work cooperatively toward
accomplishing common goals distinguishes humans from the FIGURE 1 | Selfish–selfless spectrum. The spectrum of human behavior from
extreme selfishness to extreme selflessness is plotted here as an inverted
other great apes. The survival and success of large cooperative U-Shaped curve. Social and cultural factors influencing perceptions are
societies requires most of their members to mute their innate posited to shift the curve for individuals and populations to the left (e.g., racial
selfish drives and strengthen their selfless behavior. Converging hatred) or the right (e.g., compassion training). Illustrated by Matt Hazard.
evidence that will be reviewed here strongly supports that
complex combinations of genetic and neuronal factors, including
parenting, underlie the spectrum of selfish–selfless behaviors. more prosocial than middle-class American children (Eisenberg
Given the gaps in knowledge in this multidisciplinary area of and Mussen, 1989). Finally, Robarcheck and Robarcheck (1992)
research, we propose the spectrum be initially plotted as an compared two cultures in environmentally similar conditions
inverted U-shaped curve with the x-axis representing the range but with drastically different cultures, the cooperative Semai
from extreme selfishness to extreme selflessness and the y-axis in the Malaysian rainforest and the individualistic and war-
representing the percent population at each point (Figure 1). We like Waorani from the Amazon (Robarcheck and Robarcheck,
also propose that the extreme selfishness end of the spectrum 1992). The Semai people exhibit prosocial and altruistic behavior,
is exemplified by callous-uncaring psychopaths and the extreme whereas the Waorani behave selfishly and reportedly save
selflessness end by zealous altruists that take extreme measures to themselves if faced with danger as opposed to helping members
help others. We hypothesize that the landscape and peak of the of their society or family. These and other studies implied
curve shifts for given populations based on social and cultural that societies that tend to focus on individual achievement and
factors (neuronal-based heredity) and genetic makeup. “success” result in children that are less prosocial and that exhibit
fewer altruistic tendencies. Using the Price equation, researchers
mathematically estimated that culture (neuron-based heredity)
CULTURAL AND BIOLOGICAL has more than one order of magnitude greater influence than
INFLUENCES ON THE genes on altruism and prosocial behavior at the population level
SELFISH–SELFLESS SPECTRUM (Bell et al., 2009).
Some studies have attempted to identify how the depth of
Differences in degrees of altruistic and prosocial behavior have social interactions an individual has is reflected in the gross
long been noted between cultures. In one classic study published anatomical structure of the human brain. For instance, a positive
in 1975 that observed children’s behavior across six different correlation has been recorded between the number of individuals
cultures, it was found that 100% of children between the ages a person regularly interacts with and the size of their amygdala
of 3 and 10 exhibited altruistic or prosocial behavior in Kenya, bilaterally (adjusted for total intracranial volume), but not the
contrasted with only 8% in the United States (Whiting et al., hippocampus. This correlation also held true for the number of
1975). Furthermore, this difference was linked to a cultural different social groups to which a person belongs, not just the
difference between the groups, especially in family function. number of friends with whom an individual interacts (Bickart
Prosocial children were correlated with families where the et al., 2011). The amygdala is responsible for many automatic
women contributed economically and where the children were processes that influence social cognition (Adolphs, 2009) ranging
assigned tasks within the home. Supporting these observations from the more mundane such as fear, vigilance (Whalen, 1999)
is a study by Eisenberg and Mussen (1989) that found that and alertness (Whalen, 2007) to the parsing and evaluation
Mexican children, Hopi children, and Israeli children were of facial features (Adolphs et al., 1994; Winston et al., 2002;

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

Adolphs et al., 2005; Schiller et al., 2009) in conjunction with the A correlation was also observed between offers and blood-
fusiform cortex (Hadjikhani and de Gelder, 2003; Britton et al., oxygen level dependent increases in fMRI activation of the
2008). The amygdala may play a central role in regulating an primary somatosensory cortex and other associated areas during
individual’s aversion to or propensity for social interaction based the observation of the painful hand stimulation, supporting
on the activation of the brain’s reward mechanisms during the a hypothesis of empathic behavior as a form of “self-other
reading of facial expressions and the subsequent regulation of resonance” as a result of “neural resonance” between individuals.
comfort in social situations. While undergoing fMRI the subjects were then asked to imitate
An interesting sub-population is political orientation, which faces that were displayed to them. The subjects who donated
is increasingly recognized as having a genetic as well as a more money to low socio-economic players tended to exhibit
social and cultural influence (Kandler et al., 2012; Hatemi and greater levels of BOLD increases in fMRI in the left amygdala and
McDermott, 2012), including dopamine neurochemical receptor also the left fusiform cortex which is a region responsible for facial
variant expression (Settle et al., 2010). In these sub-populations processing and implicated in empathy.
we again see the role of the amygdala in making social-based Kim et al. (2010) observed a genetic variation on the oxytocin
snap judgments when presented with images of faces. Bilateral receptor gene OXTR at rs53576 between cultures (Kim et al.,
amygdalar activation recorded by fMRI positively predicts a 2010). In individualistic European Americans a guanine (G) is
participant’s snap decision to vote for a person based solely on more prevalent at this position, but in collectivist East Asians an
appearance, a phenomenon that was observed across cultures adenine (A) is more common. Oxytocin is a neurohormone that
(Rule et al., 2010). Schreiber et al. (2013) found increasing brain is primarily involved in stimulating contractions of the uterine
activity in the right amygdala amongst Republican voters versus wall during childbirth and the milk “let-down” reflex of lactation
increased anterior insular activation in Democrats, suggesting during nursing. Oxytocin also acts on the central nervous
different limbic processes are involved in reaching decisions in system for brain development and to regulate behavior including
a risk-taking task. These findings were supported in separate maternal behaviors such as infant response and protection,
studies by Kanai et al. (2011) reported that the gray matter and other social behaviors including bonding, trusting, and
volume of the right amygdala was observed to be larger in encouraging generosity (Yang et al., 2013). Nasally administered
individuals self-described as more conservative, contrasted with oxytocin reduces fear and anxiety (Kirsch et al., 2005), increases
those self-described as more liberal who exhibited greater gray trust (Kosfeld et al., 2005), reduces xenophobic outgroup
matter volume in the anterior cingulate cortex (ACC). rejection (Marsh et al., 2017), increases monogamous behavior
The ACC is involved in many executive level brain functions, (Scheele et al., 2012), increases empathy (Sheng et al., 2013)
including reward-based decision making, error detection, and and conformity with in-group members (Stallen et al., 2012).
conflict monitoring. An example of a task that activates the error Some benefits of oxytocin beyond promoting positive social
detection/conflict monitoring function of the ACC is the “Stroop interactions include anti-inflammatory effects and indications
task” (Pardo et al., 1990). In this task the name of a color is for quicker wound healing (Gouin et al., 2010). It is being
written in a different color of ink, for example the word “RED” investigated as a treatment for the social deficits of autism (Dadds
is written in blue ink, and the subject is asked to name the et al., 2014a), however, the efficacy reported in initial studies
word and ignore the color of the ink (or vice versa). This task has been mixed with results ranging from modest benefits to no
activates the ACC. The ACC also may serve as an evaluative role observed improvements (Young and Barrett, 2015).
after effortful error commission, producing emotional distress Vasopressin has also been identified as a possible regulator
associated with the act of producing an error (Bush et al., 2000). of compassionate behavior. Human studies of individuals that
Thus, the ACC is thought to be responsible for adapting behavior exhibit strong sibling bonding (Bachner-Melman et al., 2005) and
in response to the production of errors (Luu and Pederson, pair bonding (Walum et al., 2008) have identified that increases in
2004). The perigenual region of the ACC may also play a role the length of vasopressin 1a receptor repeat sequences 1 and 3 are
in modulating the reward mechanisms in a way perceived as linked to these behaviors in these sub-groups. Vasopressin, also
gratitude at the relief of a stressor (Fox et al., 2015) and as the called antidiuretic hormone or arginine vasopressin hormone
result of positive social interactions (Van den Bos et al., 2007). (AVP), is a neurohormone that controls the antidiuretic effect
As a part of the social species, these functions may be critical in through water reabsorption in the kidneys’ nephrons and by
maintaining alliances and raising offspring through a protracted controlling the constriction of blood vessels. In terms of social
stage of dependency. behavior, central vasopressin receptors AVPR1a in the ventral
In one study (Christoy-Moore, 2016), subjects’ donations to pallidum of the prairie vole are necessary for pair bonding and
individuals based solely on profiles listing socio-economic status partner selection (Lim and Young, 2004) by activating the reward
were recorded (called the Dictator Game) and then activity levels circuitry during mating (Pitkow et al., 2001). This and other
in the subjects’ brains were measured by functional magnetic- central AVP receptors have been shown to play critical roles in
resonance imaging (fMRI) while observing video of a human social recognition and interpretation of social cues as well as
hand being punctured by a hypodermic needle, touched by a related stress pathways in knockout mouse models (Bielsky et al.,
cotton swab, or static without stimulation (called the Needle 2004; Wersinger et al., 2004).
Test). Subjects’ offers to low socio-economic status players in In addition to the strong evidence in animal studies that
the Dictator Game were positively correlated with the subject’s oxytocin and vasopressin are two neurohormones which play
own Empathic Concern score determined by questionnaire. important roles in social behavior and the resultant reward and

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

stress pathways that support those behaviors, there is increasing TABLE 1 | PCI-R: psychopathy criminal focus (APA, 2013).
research supporting the hypothesis that genetic variants of OXTR
• Core features: Callous-unemotional – lacking empathy and lacking remorse
and AVPR1a are predictive of humans displaying greater degrees for mistreating others.
of altruistic, empathic and compassionate behavior traits within • Frequently breaking the law, being arrested.
population sub-groups. For example, Poulin et al. (2012) have • Pervasive dishonesty, chronic lying.
reported that the amount of individual involvement in charitable • Dysfunctional planning.
activity and civic duties correlated with genetic variants. As • Impulsive, irritable and aggressive behavior.
expected, it was found that those with the OXTR rs53576 G • Fearless, reckless and irresponsible, endangering self and others.
to A variation or AVPR1a RS1/RS3 long to short variation
were more likely to exhibit “prosocial” behavior by being more
trusting of strangers, contributing more to charitable activities
a monolithic disorder (qualitative), or is it a syndrome
and participating in more civic duties.
with multiple interacting factors determining the extent and
phenotypic expression (quantitative)? To more fully evaluate the
hypothesis of multiple interacting factors, an alternate rating scale
EXTREME SELFISHNESS: CRIMINAL to the PCL-R has been developed, the Psychopathic Personality
PSYCHOPATHY Inventory-Revised (PPI-R, see Table 2) designed and validated to
measure more affective and interpersonal traits and to be used
Callous-unemotional criminal psychopaths epitomize extreme
in both criminal and non-criminal populations without a priori
antisocial behavior. These individuals are characterized by
assumptions of antisocial and criminal behavior (Skeem et al.,
aggression and violence with a long criminal record and frequent
2011; Dutton, 2016; Sorman et al., 2016).
incarceration. Their core behavioral pattern of pervasively
While the two different rating scales overlap in measures
violating the rights of others without remorse can begin as early as
such as meanness (e.g., callous and unemotional, coldhearted),
3 years of age and continue into adulthood (Hare, 2006; Gao and
antisocial behavior (e.g., pervasive dishonesty, Machiavellian self-
Raine, 2010; APA, 2013). In the United States, they are estimated
interest) and poor planning skills, PPI-R includes the positive
to represent 16% of male prisoners (Kiehl and Hoffman, 2011).
traits of boldness (social dominance, immunity to stress and fear).
In England and Wales, the estimates are lower, close to 8% of
While all unsuccessful psychopaths are by definition criminals,
men and 2% of women (Coid et al., 2009b), perhaps due to
as mentioned before, successful psychopaths on the PPI-R scale
cultural differences between the countries. Serial killers fall into
are found in politics, medicine and business. Their actions range
this category. However, by maintaining an outwardly normal
from criminal to courageous, as evidenced by the high PPI-R
persona, they can often evade detection and arrest for periods
scores of national leaders of World War II: Franklin D. Roosevelt,
running into decades.
Winston Churchill, and Adolph Hitler (Dutton, 2016). Roosevelt
The spectrum of personality disorders classified as
and Churchill were powerful leaders whose bold, hardnosed
psychopathic is much broader than those on the extremist
(coldblooded) actions were instrumental in the survival and
criminal end. Psychopaths can be separated into two groups –
success of their social order; Hitler’s leadership epitomizing
unsuccessful and successful (Gao and Raine, 2010). The
callousness, lack of remorse and blame externalization was
unsuccessful are the callous-uncaring criminals. Successful
disastrous for all of Europe and led to notorious crimes against
psychopaths are a more diverse group ranging from ruthless con
humanity.
artists to leading statesmen (Dutton, 2016). Both unsuccessful
As successful psychopaths can intelligently conceal their
and successful psychopaths can exhibit varying combinations of
psychopathic traits, their number in the population is difficult
traits, which collectively predict their behavioral patterns. With
to detect. In one large population survey, the prevalence of
the legal and societal problems created by criminal psychopaths,
successful (i.e., no criminal record) psychopathic individuals
most research has been focused on defining their psychological
living in households in England was 0.6% (Coid et al., 2009a). In
features and neurobiology. The current criteria for determining if
the professional world of politicians, businessmen, doctors and
someone is a criminal psychopath is the Psychopathy Checklist-
lawyers, the number may be much higher. In their book Snakes
Revised (Hare, 2003; Babiak and Hare, 2006), which is crafted
in Suits: When Psychopaths go to Work, industrial psychologist
for clinical and legal use, emphasizing antisocial and criminal
behaviors. It is used worldwide and its influence is seen in
the gold standard for clinical diagnosis, the 5th Edition of the
American Psychiatric Association’s Diagnostic and Statistical TABLE 2 | PPI-R: psychopathy positive and negative features (Skeem et al., 2011;
Dutton, 2016).
Manual of Mental Disorders (APA, 2013) where psychopathy is
described as a synonym for Antisocial Personality Disorder (see • Coldblooded
Table 1). • Powerful social dominance
As Hare developed his PCL-R as a research tool based largely • Fear immunity
on his experience in analyzing criminals, its use more broadly • Stress immunity
• Machiavellian self-interest
in formulating public policy, in business and in conducting • Rebellious non-conformity
unbiased social research is controversial (Skeem et al., 2011). • Blame externalization
Also, it has raised a major scientific issue. Is psychopathy • Carefree living (no planning)

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Babiak and criminal psychologist Hare (Babiak and Hare, 2006) social processing and behavior regulation (Anderson et al.,
estimated 3.5% of professionals in business possess strong 1999; Grossman, 2013). In individuals with pronounced conduct
psychopathic traits. While some professionals with psychopathic control problems, numerous studies have shown the amygdala
traits are criminals, others benefit the social order by boldly is smaller along with less gray matter volume in the frontal and
leading changes needed for cultures to adapt to ever changing temporal cortices (Yang et al., 2010; Rogers and De Brito, 2016).
environmental, economic, and political conditions. Hypoactive amygdala responses to stimuli of others in distress
are characteristic of children with the callous-unemotional trait
and associated with aggressive behavior (Lozier et al., 2014).
NEUROBIOLOGY OF PSYCHOPATHY Humans with bilateral amygdala lesions have impaired learning
of fear and responding to eminent danger (Bach et al., 2015;
Dysfunctional emotional processing is a defining feature of Klumpers et al., 2015). Bilateral amygdala lesions in rhesus
psychopathy (Anderson et al., 2017), from lacking empathy monkeys have significantly blunted stress responses (Raper et al.,
to possessing immunity to stress and fear. Meta-analyses of 2013). These findings strongly link the behavioral traits of the
26 studies found emotional recognition of facial expressions callous-unemotional trait, boldness, and fear/stress immunity to
and vocal cues was significantly impaired in young and adult amygdala functions.
psychopaths for all of the basic emotions: anger, disgust, fear, The hypothalamus is intimately involved as the control center
happiness, sadness, and surprise (Dawel et al., 2012). Their of the brain for autonomic responses and regulation of sex
inability to recognize fear and sadness was especially pronounced, hormones and the secretion of oxytocin, cortisol, and vasopressin
but they also exhibit reduced neural response to laughter into the bloodstream. Low oxytocin levels have been linked
(O’Nions et al., 2017). Such blunted emotions affect perceptions, with callous-unemotional scores in adolescents (Levy et al.,
thought processes and actions toward others, fostering both 2017). Supporting this link are other studies indicating that
boldness and lack of remorse. Dysfunctional emotions also affect inactivation of the oxytocin receptor by DNA methylation is
another trait of criminal psychopaths – deeply flawed reasoning, correlated with an increased risk of callous-unemotional traits
including moral judgment. (Cecil et al., 2014). Children and adolescents with the callous-
Three of the sites in the brain responsible for criminal unemotional trait exhibit reduced cortisol response (von Polier
psychopathic behavior are also principal components of the et al., 2013; Grotzinger et al., 2018) perhaps explaining increased
neural circuitry for normal social-emotional processing: the boldness/impulsivity, and are at high risk for developing
prefrontal cortex (PFC), amygdala, and hypothalamus (Figure 2). into criminal psychopaths (Kahn et al., 2013; Kimonis et al.,
Psychopathic behavior resulting from injury or disease implicates 2016). As discussed earlier, oxytocin and vasopressin are two
the ventromedial PFC (vmPFC) as a critical node for prosocial neurohormones that have essential roles in social behavior and
behavior; its dysfunction resulting in antisocial behavior the resultant reward and stress pathways that support those
(Anderson et al., 1999; Barrash et al., 2000; Trebuchon et al., behaviors (Poulin et al., 2012).
2013). The enlarged prefrontal cortex is the neocortical (i.e., The neural circuitry for the Impulsive-Antisocial dimension
evolutionarily newest) region of the human brain responsible for of psychopathy overlaps with that for Boldness, but differs in
top down, executive control; while the amygdala is the part of important details. The size of the striatum, a major component
the allocortical (i.e., evolutionarily old) cortex that, as discussed of the basal ganglia, is larger in Impulsive-Antisocial individuals
earlier, integrates sensory and acquired information, including (Korponay et al., 2017), especially the putamen and the nucleus
facial features, to assess threat levels. In the mammalian brain, accumbens in the ventral striatum, the reward center of the brain
the PFC is richly networked with the amygdala (McDonald (Figure 3).
et al., 1999), with neurons in the cerebral neocortex sending Dopamine release from ventral tegmental area dopamine
fibers to connect with neurons in the amygdala embedded in neurons innervating the nucleus accumbens is an essential
the rostral temporal lobe (Stein et al., 2007). Like most neural component of the reward circuitry (Sesack and Grace, 2010;
assemblages in the brain, it is a two-way street with amygdaloidal Kahn and Shohamy, 2013). In functional MRI studies, the
neurons sending fibers to the cerebral cortex. The amygdala in ventral striatum including the nucleus accumbens displays robust
turn is richly interconnected with the hypothalamus (Herman, activation in criminal psychopaths in game tasks involving
2012), another evolutionarily ancient brain region that regulates rewards (Pujara et al., 2014). The nucleus accumbens is a major
homeostasis and autonomic nervous system activity (Jansen et al., component of the limbic system (Morgane et al., 2005), the
1995) and controls neuroendocrine functions including secretion part of the human brain that provides emotional processing
of oxytocin and vasopressin into the systemic circulation (Carter, and motivational information to the enlarged, more deeply
2014). layered areas of the prefrontal cerebral cortex (Shnitko and
The association between medial prefrontal cortex (PFC) Robinson, 2014). Other interacting centers include the amygdala
dysfunction and psychopathic behavioral features including and hippocampus (de la Mora et al., 2010).
lack of empathy and remorse, dishonesty, and poor planning As recently emphasized by Reidy et al. (2017), reward-
and decision-making skills, has been extensively documented dominant learning and decision making in callous-unemotional
since the index case of Phineas T. Gage in 1848 (Harlow, individuals with strong Impulsive-Antisocial traits can explain
1868; Damasio et al., 1994). Since then, there has been an their extremely violent behavior, their hair-trigger response for
abundance of research supporting the role of the PFC in evoking rage or anger (the fight component of “Fight or Flight”

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

FIGURE 2 | Prefrontal cortex-amygdala-hypothalamic circuitry. The prefrontal cortex-amygdala-hypothalamus axis has a pivotal role in social-emotional processing.
Developmental disorders and injuries effecting its neural assemblages and circuitry can lead to antisocial behaviors characterizing psychopathy. (A) In this
parasagittal view of the human brain, the spatial relationships and neural connectivity between the prefrontal cortex (PFC), amygdala (Amy), and hypothalamus (Hyp)
are illustrated. Lesions involving the ventromedial PFC (vmPFC) are especially disruptive of prosocial behavior. Note the central role of the amygdala in the circuitry
linking the prefrontal cortex and hypothalamus in the emotional processing network. Also see its intimate integration of the amygdala with the head of the
hippocampus (Hip), which initiates and consolidates cognitive memory and learning processes in the brain. (B) Here is a schematic based on the generic mammalian
brain to illustrate the multiple actions taken by the hypothalamus when a “Fight or Flight” response is triggered by cortical-amygdala interactions signaling high levels
of risk or immediate danger, including life or death situations. Neurons in the hypothalamus terminating in the pituitary release oxytocin (OT), vasopressin (VP) and
adrenocorticotropic hormone (ACTH) into the systemic circulation. The sympathetic nervous system is fully activated via the hypothalamus, including by a direct
neural projection to the adrenal medulla stimulating release of epinephrine (EPI, adrenalin) and norepinephrine (NEP, noradrenalin) into the blood stream. ACTH
stimulates the release of the stress hormone cortisol (COR) from the adrenal cortex. The physiological responses include hyperarousal, focused vision, increased
heart rate and blood pressure, blood shunted to the muscles, and suppression of digestion and appetite. Illustrated by Matt Hazard.

FIGURE 3 | Dopamine reward system of the brain. (A) Dopamine neurons in the ventral tegmental area (VTA) directly innervate the nucleus accumbens (NAc),
prefrontal cortex (PFC), amygdala (Amy), and hippocampus (Hip) (de la Mora et al., 2010; Kahn and Shohamy, 2013; Shnitko and Robinson, 2014). As in most
neural networks, connectivity between the nuclei goes both ways. Dopamine release from the VTA promotes feelings of satisfaction, pleasure and euphoria,
rewarding and motivating behavior. Dopamine release from the substantia nigra in the striatum modulates motor functions. (B) While the neurocircuitry modulating
the VTA and NAc is complex, major projections from the PFC, Amy and Hip to the VTA and NAc have been identified (Sesack and Grace, 2010). This is consistent
with known modulation of reward system dopaminergic activity being influenced by goal-directed behavior (PFC), emotions and feelings (Amy) and
experience/memories (Hip) (Sesack and Grace, 2010). Illustrated by Matt Hazard.

behavior). In these individuals, rage and impulsivity with reduced The absence of normal fear and stress responses is analogous
fear from the amygdala evokes pleasure – dopamine release in the to removing the brakes on a bulldozer. Boldness and greatly
nucleus accumbens. muted fear with positive reinforcement from the reward system

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of the brain is the result. For criminal psychopaths, it leads of callous-unemotional behavior in their adopted child. The
to clashing violently with others and taking risks that lead to effect was dose-dependent, adoptive mothers with high positive
incarceration, debilitating injuries or death. reinforcement completely buffered the expression of the callous-
unemotional behavior at 27 months (Hyde et al., 2016; Viding and
Pingault, 2016). Follow-up studies over time will be extremely
NATURE VERSUS NURTURE IN important to assess the efficacy of early positive parenting on
PSYCHOPATHY adolescent and adult behavior patterns.
Even with the caveat that longer longitudinal studies are
Based on parent reported data on 5092 twins, genetically modeled needed, the malleability of callous-unemotional behavior in early
inheritance for the core feature of psychopathy – callousness childhood is encouraging. But as a developmental neural disorder
and unemotional trait – was 70% (Henry et al., 2016). A smaller with structural neuroanatomical abnormalities (Cope et al., 2014)
more recent study examining the reliability of parent reported and impaired functional connectivity (Harenski et al., 2018),
data refines the estimate to 47% (Moore et al., 2017). For the how long is the window of opportunity open for therapeutic
traits of Boldness and Impulsive-Antisociality, twin studies have intervention for criminal psychopaths? Working with juvenile
reported inheritance in the 40–50% range (Blonigen et al., 2005) delinquents, over half of whom had committed a serious violent
and indicating the two traits were not linked genetically and differ felony, a program at the Mendota Juvenile Treatment Center in
in their neurobiology. Wisconsin using intensive therapy balancing punishment for bad
Some progress has been made in identifying genes associated behavior with rewards for improved behavior was able to reduce
with features of psychopathy. Consistent with data reported the number of crimes by over 35% perpetrated by the trainees
throughout this review that oxytocin has a prominent role in over a 4–5 years period after release, compared to a treatment-as-
promoting prosocial human behavior, two independent studies usual control group (Caldwell and Van Rybroek, 2005; Caldwell,
have recently found a high association between an oxytocin 2011). While the effects on violent behavior were impressive,
receptor gene and callous-unemotional traits (Beitchman et al., there remained a significant risk for aggressive behavior injuring
2012; Dadds et al., 2014b). Endogenous oxytocin is important others.
in neural development including neural circuitry (Carter, 2014), The Mendota Center approach of effectively reinforcing
making it difficult to predict the effects from administration of the reward center of the brain for improved behavior, while
exogenous oxytocin to the adult brain after critical periods in providing negative reinforcement for bad behavior, is now being
brain development. Initial studies indicate nasal administration tested elsewhere for younger adolescents with strong callous-
of oxytocin increases aggressive behavior in normal adults unemotional traits (Hagerty, 2017). However, treatments for
(Ne’eman et al., 2016) and adults with antisocial personality adult criminal psychopaths have been notoriously ineffective and
disorder (Alcorn et al., 2015). upon release 90% commit another violent crime within 20 years
(Anderson and Kiehl, 2014).
Role of Neuron-Based Heredity in
Psychopathy
To what extent can neuronal-based heredity – learned EXTREME SELFLESSNESS: ZEALOUS
societal and cultural traits – compensate for strong genetic ALTRUISM
psychopathic predispositions? This acquisition of social and
cultural information begins before birth (Partanen et al., 2013) Placing the interests of others above one’s own safety occurs
as newborns recognize their mother’s voice and can distinguish so regularly in the United States and the rest of the world
it from a stranger’s voice (Beauchemin et al., 2011). Prenatal that it garners little media attention (Ricard, 2013, 2015). Only
development and functioning of neural systems is evident after when there is serious injury or death of the Good Samaritans
birth with the pattern of crying of newborns shaped by their does it make the news, such as in May 2017 when a crazed
native language (Mampe et al., 2009). Positive parental support man approached two young women on a commuter train
and maternal behavior is exceptionally important during these in Portland, Oregon brandishing a knife and screaming anti-
critical periods. Chaotic home environments, negative parental Muslim insults. Three strangers rushed to rescue the girls. Two
behavior and mothers with strong callous-unemotional traits died and the third was seriously injured (Kristof, 2017). As
can affect their fetus’s and infant’s emotional and cognitive the list of Carnegie Medal recipients for Extraordinary Civilian
development (Fontaine et al., 2011; Hyde et al., 2016; Viding and Heroism shows (CarnegieHero.Org, 2017), altruists range from
Pingault, 2016). adolescents to aged adults. Some are very young like 10 year-
In a study of 561 children adopted within several days after old Kiera Larsen who saved a 2-year old child from being run
birth where severe callous-unemotional maternal behavior was over by a car that then struck and killed her. They can be
replaced by strong positive support, major effects were found in old, like 72 year-old Louis Scharold who braved intense heat
altering behavior (Hyde et al., 2016). Having a biological mother from burning, wrecked trucks to reach through the broken
with severe callous-unemotional behavior predicted the same windshield of one vehicle to pull the dazed driver to safety.
traits in their children at 27 months of age, even though they had Twelve of the 94 Carnegie Medal Recipients in 2016 lost their
not been parenting them after adoption. Positive reinforcement lives in trying to save others. Again, routine altruistic actions
by the adoptive mother significantly mitigated the expression are commonplace and seldom make the news, but extraordinary

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

risks taken by some can and do lead to injury and death. and altruism. A linkage that has been repeatedly replicated
These zealous altruists on the extreme end of the spectrum are (Persson and Kajonius, 2016) and further modeled and linked
those who take extreme measures to help others, unnecessarily with oxytocin by Zak and Barraza (2013). The second factor
placing themselves in harm’s way, such as anonymous living is punishment of those violating social norms (Fowler, 2005).
kidney donors that partake in surgery to donate an organ to an The efficacy of punishment as in promoting cooperation has
unrelated and unknown recipient they will never meet (Tong been controversial. However, a meta-analysis of punishment
et al., 2012). and cooperation in 18 societies found punishment strongly
Altruism can be impulsive suggesting instinctive reactions promoted cooperation in societies with high trust levels (Balliet
as in the preceding cases, or premeditated by choosing to help and Van Lange, 2013). Also as Mussweiler and Ockenfels (2013)
others in ways that are knowingly risky indicating involvement have demonstrated, perceived similarity promotes altruistic
of executive functions, such as the actions of David Eubank, cooperation as well as evoking increased punishment for norm
the American Aid Worker who rescued a young girl, the lone violations. The result, they suggest, enhances the ability for
survivor of about 70 civilians massacred by ISIS fighters as similar individuals to build strong, stable socially cooperative
they tried to free Mosul in June of 2017. Braving sniper fire groups.
with some support from Iraqi and US Forces, Eubank ran into
the street, picked the girl up and brought her back to safety
(Yuccas, 2017). Eubank has repeatedly chosen to go to war- NEUROBIOLOGY OF ALTRUISM
ravaged areas in Asia to aid children and others in need. Less
dramatic, but equally extreme premeditated acts of generosity Implicit mind reading skills (gene-based) are present by the first
are those of altruists who donate one of their kidneys to help 4–7 months of life with normally developing infants making
an unknown anonymous patient (Marsh et al., 2014), placing face-to-face communication that activates the medial prefrontal
their own lives at risk from complications of elective surgery and cortex (Grossman et al., 2008; Kovacs et al., 2010; Urakawa et al.,
the removal of an organ. Other less risky altruistic premeditated 2015). Most or all neurocognitive mind reading skills are acquired
actions include being a blood donor or donating bone marrow for and strongly shaped by culture (neuron-based), with the early
transplantation. stages of learning similar to those of learning to read (Heyes and
Thus, the conundrum of altruism – taking risks by placing the Frith, 2014). Infants are very vulnerable, so development of the
interests of others, often strangers, beyond one’s self-interest – ability to distinguish between those who can help versus those
seems to directly violate the “survival of the fittest” principle of who may pose a risk is essential. Strong evidence from many
gene-based evolution. Darwin noted both sides of the issue in research groups indicates that the majority of infants as early as
The Descent of Man. He astutely recognized that selfishness was 6–10 months of age prefer and selectively approach individuals
a roadblock to human social evolution, “Selfish and contentious displaying intentional prosocial behavior (Hamlin and Wynn,
people will not cohere, and without coherence nothing can be 2011; Holvoet et al., 2016; Van de Vondervoort and Hamlin,
effected.” However, Darwin continued, writing, “He who was 2017). Also by 1–2 years of age, simple reciprocal interactions
ready to sacrifice his life, as many a savage has been, rather than elicit an early form of altruistic behavior, the child helping the
betray his comrades, would often leave no offspring to inherit his experimenter or a stranger obtain an object clearly out of their
noble nature” (Darwin, 1871). Darwin (1871) proposed that as reach (Barragan and Dweck, 2014). By 5 years of age, children
ancestral human reasoning and foresight powers increased, the are capable of sharing with others and anticipating reciprocation
benefits of reciprocal social assistance would become obvious and (Sebastian-Enesco and Warneken, 2015).
gradually lead to inherited reciprocal benevolence. Altruism goes well beyond reciprocation by compassionately
Darwin seems to have been justified, as just discussed there is helping a stranger with no apparent self-benefit and at some
strong evidence for both instinctive and cognitive benevolence in risk to one’s own being. Neuroimaging studies have provided
our species. This evolution has occurred thanks to a capability important insights into the neural networks underlying the
of the mind Darwin did not anticipate. Namely, our species behavioral linkage between empathy and compassion. As defined
possesses enhanced mind-reading skills to understand our own by de Waal and Preston (2017), empathy is a “term for all
thoughts and emotions and what others are thinking and feeling processes that emerge from the fact that observers understand
(Heyes and Frith, 2014; de Waal and Preston, 2017). Affective others’ states by activating their own personal, neural, and
perception of other’s emotions includes the six basic emotional mental representations of that state.” Empathy then is a
states visualized by facial expressions and body language: anger, passive state of feeling. Physical pain or distress, and empathy
fear, surprise, sadness, disgust, and happiness. Feeling and from witnessing pain both activate the same higher brain
understanding the emotions of others, the recognition of signals areas, the anterior insula and anterior to mid cingulate cortex
of need, sets the stage for perception-based actions such as (Figure 4) (Lamm et al., 2007, 2011). Depending on the
benevolence and compassion. type of distress, other brain areas such as the primary motor
With mind-reading skills at work, two major interactive and somatosensory cortices are recruited to simulate in the
factors appear to be crucial for promoting and maintaining broad observer the neural activity in distressed individual: a vivid
levels of cooperation within human populations. The first, as example of the continuing theater of the mind envisioned
hypothesized by Batson et al. (1981, 1983), Toi and Batson (1982) by the founder of modern psychology William James over
and tested in a series of studies, is a strong link between empathy 100 years ago where one’s own thoughts and sensations

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

FIGURE 4 | Active cortical sites for fear, distress, and empathy. Two deep cortical regions, the anterior insula and anterior cingulate cortex are strongly activated
when feeling fear and empathy. Both are strongly interconnected with the amygdala (Stein et al., 2007). (A) The insula lies beneath the temporal and cortical lobes
and can be seen by separating the two lobes. (B) The anterior cingulate gyrus is the deepest cortical region of the prefrontal cortex (PFC) as seen in this sagittal
section, and caps the anterior corpus callosum. Illustrated by Matt Hazard.

are blended with ongoing experience to produce emotions between Zealous Altruists (individuals who had donated one
and feelings. Empathy for another in extreme pain can be of their kidneys for transplant recipients) and Criminal
extremely painful (Fitzgibbon et al., 2010; Ricard, 2015). Psychopaths. Brain size can be larger than normal controls in
Intense and repeated exposure to distress can lead to severe zealous altruists and, even controlling for the brain volume, the
emotional and health problems including empathetic distress right amygdala is larger (Marsh et al., 2014). As reviewed earlier,
and post-traumatic stress syndrome (APA, 2013; Klimecki et al., in psychopaths with conduct control dysfunction, the amygdala
2014). is smaller along with less gray matter volume in the frontal
As opposed to the passive state of empathy, compassion is and temporal cortices (Yang et al., 2010; Pardini et al., 2014;
taking action to help others, including other species, in distress. Rogers and De Brito, 2016). In contrast to psychopathy where
Synonyms for compassion that help define it are benevolence, responses to all facial expressions of emotion are muted, altruists
kindness and sympathy. Compassionate actions activate the show an enhanced responsiveness to fearful facial expressions
reward system of the brain, the ventral striatum and the and diminished responsiveness to anger (Marsh et al., 2014).
dopaminergic ventral tegmental area, as well as the medial The neural pathways involved in compassion are similar to
orbitofrontal cortex (Klimecki et al., 2014). The positive affect those for impulsive-antisocial behavior. In this instance, prosocial
from compassion not only reinforces benevolent behavior, but compassionate behavior rather than antisocial behavior activates
can also calm painful empathetic feelings (Figure 5). the dopamine reward system of the brain. The same neural
Neuroimaging studies on adult Europeans making decisions systems are engaged (hippocampus, ventral striatum and ventral
on altruistic giving have identified two strongly engaged tegmental area, prefrontal cortex and amygdala). The major
brain areas. Activity in anterior insula predicted generosity in difference between prosocial and antisocial behavior is likely
individuals influenced by emotional empathy, while activity embedded in the perception of social order. This difference
in the temporoparietal cortical junction was associated with is wittily broached in a letter by Walpole (1769) in which he
cognitive empathetic giving (Tusche et al., 2016). Another study declared, “this world is a comedy to those that think; a tragedy
taking a similar approach testing young European adults reported to those that feel – a solution of why Democritus laughed and
that volume of gray matter in the right temporoparietal cortical Heraclitus wept.” For altruists, the full capability for processing
junction was strongly positively correlated with the maximal and integration of sensory and acquired information in the
acceptable cost for an altruistic action (Morishima et al., 2012). reading and feeling of emotions of others engenders taking
The results from both studies are supportive of the concept of positive actions – compassion – that mitigates the altruist’s own
altruistic potential being a common feature in populations and distress and reflexively activates the reward system. With the
that can be evoked by empathetic feelings. muted neurocircuitry for basic emotions in criminal psychopaths,
Another approach for identifying brain areas engaged in taking action in the form of violent aggression actives the
altruistic giving is that taken by Marsh et al. (2014) using anger/fight component of the Fight or Flight response reflexively
neuroimaging to quantify structural and functional differences activating the reward system.

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

FIGURE 5 | Benevolence pathway. (A) Empathy involves literally feeling another’s pain. An individual with empathic responsiveness upon seeing and or hearing
others in pain mirrors that pain in their brain, activating the same higher cortical brain areas activated by fear, the anterior insula and mid-to-anterior cingulate cortex.
Intense exposure to a stressful event or repeated exposure to stress in others can lead to burnout, empathy fatigue or PTSD. (B) Compassion activates the reward
system of the brain and can significantly calm empathetic feelings of fear and pain. Therefore compassion and benevolence elicit positive feelings. Altruism not only
benefits the recipient, but also benefits the altruist by rewarding their behavior with feelings of satisfaction. Illustrated by Matt Hazard.

NATURE VERSUS NURTURE IN have high non-social anxiety. With cognitive deficits and overly
ALTRUISM trusting of others these individuals cannot live independently.
Several hundred genes, many of them rare copy variations,
Given that altruistic behavior can be expressed by large segments have been implicated as risk factors for dysfunctions in
of the population as discussed earlier, the genes underlying communication and mind reading that characterize autism
altruism may be commonplace. This includes genes for central spectrum disorders (Pinto et al., 2014; Sahin and Sur, 2015).
dopaminergic systems engaged in the reward system and genes The large number is consistent with the broad heterogeneity of
for oxytocin receptors that promote development of the social symptoms and their expression in autism. While alterations in
brain with strong capabilities for communication and mind oxytocin stimulatory proteins, oxytocin plasma levels and genetic
reading of emotions (Donaldson and Young, 2008; Carter, 2014; variance in oxytocin receptors have been reported as risk factors
Heyes and Frith, 2014). for autism (Jacobson et al., 2014; LoParo and Waldman, 2015),
If genes underlying altruism are the norm, then it can clinical trials on the efficacy of oxytocin therapy has found only
be predicted that gene variants and mutations resulting modest benefits or no positive effects (Young and Barrett, 2015).
in dysfunctional and antisocial behavior can be used to Collectively, the genetics underlying psychopathy, Williams
identify gene networks that are good candidates for promoting disease and autism indicate that no one gene is responsible for the
altruistic behavior. With the Callous-Unemotional trait found development of the human prosocial brain, but a broad network
in individuals at high risk for violent criminal behavior, genetic of interacting genes found in normal populations set the stage for
variants in the oxytocin receptor have been identified as discussed the second system of heredity (neuron-based) to sculpt prosocial
earlier. Dysfunctional social behavior is also found with the brain functions.
overexpression of oxytocin. Williams Syndrome, which results
from the loss of 28 genes, features dysregulation of oxytocin and Role of Neuron-Based Heredity in
vasopressin secretion by the hypothalamic-pituitary system (Dai Altruism
et al., 2012). Baseline plasma levels of oxytocin are three-times The human genome containing around 20,000 protein-encoding
higher and vasopressin levels 0.30% higher in Williams Syndrome genes can provide the basic blueprint for brain development,
than in controls. Individuals with Williams Syndrome possess but training and experiences in the early years from infancy
cognitive deficits with behavior characterized by diminished through childhood are crucially important in sculpting brain
social anxiety and fearfulness, readily approaching, socially development and function. As discussed earlier, prosocial
interacting with and trusting strangers (Jarvinen et al., 2013). behavior is displayed by most infants and preschool children.
However, they experience difficulty interacting with peers and Culture plays a major role in enhancing and strengthening

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

prosocial behavior. Even where genetic inheritance of the callous- human subjects 5 days after training (Leiberg et al., 2011),
unemotional trait is a significant risk factor for developing suggesting long-term processing and learning through reward
criminal psychopathic behavior, especially in chaotic, uncaring mechanisms. Reflecting on gratitude increases scores on a
environments, expression of risky behavior can be muted by early self-report measure of altruistic values and coincides with
adoption and raising with strong positive parenting. increased BOLD fMRI activation in the nucleus accumbens
The typical experience for a newborn is rapid bonding with a and vmPFC (Karns et al., 2017) indicating involvement of the
loving mother providing intensive high-attentive care. When this mesolimbic dopamine pathway for reward and reinforcement
does not happen and there is profound social deprivation early in learning of altruistic behavior (Strobel et al., 2011). Further
life, such as institutionalization in an orphanage, prosocial brain supporting the role of social learning as important in the
development is severely compromised. Connectivity between the cultivation of prosocial behavior are studies linking oxytocin,
prefrontal cortex and amygdala is altered and the amygdala- previously described for its prosocial and parental functions,
hypothalamic-pituitary stress axis affected (Gee et al., 2013; with dopamine circuitry. Oxytocin receptors and dopamine
McLaughlin et al., 2014). The constellation of problems found receptors coexist in the striatum, medial PFC, substantia
in institutionalized children include: smaller brain size with nigra and ventral tegmental area (Skuse and Gallagher, 2009).
reduced cortical thickness, deficits in cognitive and language Intranasal oxytocin in normal humans appeared to increase
functions, problems with emotional regulation, and increased the reward for reciprocated cooperation through increased
risk for psychotic symptoms (Tottenham et al., 2010; McLaughlin activation of the dopamine-activated, reward-linked nucleus
et al., 2014; Trotta et al., 2015; Bick and Nelson, 2017). accumbens during repeated iterations of Prisoner’s Dilemma
From these studies we see that development plays an game (Rilling et al., 2012) which supports the role of oxytocin
important role in cultivating behavior, and that early intervention and dopamine learning pathways in trust and reciprocation
can help recover normal development, even impacting adolescent behavior.
criminals. How much of this is learning and how much is Thus social and cultural behaviors and activities are
developmental determinism? Studies of economic games such as mechanisms for not only training the brain beginning in
the Prisoner’s Dilemma indicate wide differences in the display prenatal life, they are also principal components in determining
of prosocial behavior in single and iterative play (Fehr and brain development and dopaminergic reinforcement learning
Schmidt, 2003). However, a study of 102 adults participating in in the adult. Empathy and compassion are feelings with basic
a repetitive Social Gambling Task indicated that an individual’s genetic and neural underpinnings crucial for the development of
ability to learn how their actions impacted another’s outcome large interacting social communities characterizing our species.
led to more prosocial behavior (Kwak et al., 2014). In this Successful cultures have strong and effective implicit and explicit
context, learners were defined as those who made choices mechanisms for promoting and enhancing empathetic and
resulting in economic gain, whether for themselves or others, compassionate behavior. Empathy and compassion are core
and is mathematical in nature. On a neuroscientific basis, values in most, if not all, of the world’s major religions. Buddhist
learning occurs with the release of dopamine in the reward methods for training the mind through meditation and yoga
and reinforcement centers of the brain including regions of (Tomasino et al., 2014) are an example of positive approaches
the striatum, such as the nucleus accumbens, from the ventral to enhance empathy and compassion that have been secularized
tegmental area and substantia nigra. Rodents have been observed and entered mainstream Western culture and medicine through
to learn the conditions of an experimental shock more quickly mindfulness practices (Gotink et al., 2015).
after vicariously observing other rodents receive the shock during While this review has focused on those populating the
such conditioning experiments. These rodents vicariously learn extremes of the social, behavioral, and cognitive spectrums, the
the conditions of the experimental shock more rapidly if they question remains as to whether individuals within a cultural
also have experienced the shock for themselves, regardless of norm can alter their behavior to become more compassionate
whether that shock was experienced within the context of the and display less selfish behavior. For this non-clinical cohort
conditioning experiment or not (Sanders et al., 2013; Lahvis, there exists an interesting non-clinical approach encompassed
2017). Rodents that had these vicarious learning experiences by mindfulness-based and compassion meditation. In one
while hearing pain-induced vocalizations in others exhibited BOLD fMRI based study of expert and novice compassion
increased activation of both dopamine and serotonin circuitry meditators, an increase in activity was observed in the ACC,
and the ACC (Kim et al., 2014) suggesting both empathy amygdala, and the insular cortex (among other regions) of
and learning through limbic systems and dopaminergic reward expert meditators during meditation compared with non-
mechanisms. These studies on vicarious or empathic learning meditative rest in response to negative emotional sounds (Lutz
are supported by studies in humans showing experience of a et al., 2008), indicating that compassion meditation increased
painful stimulus increases empathy in human observers (Eklund activation of these emotion-processing limbic regions that
et al., 2009; Preis and Kroener-Herwig, 2012) which coincide are connected to the prefrontal cortex (also see Fox et al.,
with BOLD fMRI data indicating that the perception of pain 2016). These include regions implicated in the selfish–selfless
in others is neurologically similar to the actual sensation of spectrum as outlined previously in this text. The degree
pain (Preis et al., 2015). Participation in the Zurich Prosocial of activation of these regions also correlated with the self-
Game, a computer-based compassion training game that requires reported depth of meditation and the degree of meditative
cooperation, has been shown to increase helping behavior in training, indicating that additional experience activates these

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Sonne and Gash Neurobiology of the Selfish–Selfless Spectrum

regions of the brain to a greater degree. Some groups have social debate over “universal selfishness” or “universal goodness”
attempted to bring this practice to the clinical psychology setting characterizing human behavior. Both positions are partial truths
(Fox et al., 2016). One study found that 12 weeks of mindfulness- based on the components of the Selfish–Selfless Spectrum being
based intervention with compassion meditation in a group with observed. As a lens into the social brain, the extremes of
social anxiety disorder resulted in a significant improvement the Selfish–Selfless Spectrum defined by callous, unemotional
in social anxiety symptoms, depression, social adjustment, and psychopaths and dynamic, zealous altruists reveal the importance
enhancement of compassion, all compared to a control group of both genetic and neuron-based heredity systems and reward
that was placed on a waiting list at the beginning of the study processes in strongly influencing actions toward others and
(Koszycki et al., 2016). cooperative behavior. Critically, individuals with genes associated
In the general population, mindfulness-based practices have with developing dangerous social disorders such as callous,
been reported to promote a plethora of effects on the whole body: unemotional traits have the potential to modify those conditions
reducing stress hormones, reducing inflammation, promoting using cognitive therapeutic interventions (e.g., strong positive
pain relief and wound healing (Hofmann et al., 2011; Lutz et al., parenting, compassion training) to change where they reside
2013; Zeidan et al., 2015; Rosenkranz et al., 2016). Other forms on the social spectrum. Evidence from population groups
of meditation including concentrative eye-gazing and controlled ranging from incarcerated juveniles, adopted children, twins,
breathing have been shown to result in voluntary activation and meditators point to the important role of neuroplasticity
of components of the sympathetic nervous system, changes in and reward learning circuitry in forming and reforming of
plasma catecholamine and serum cortisol concentrations, and neural connections that determine our behavior. Success with
an attenuation of the innate immune response as measured by treatment programs promoting positive behavior via the brain
plasma cytokines (Kox et al., 2014) and IL-6 markers (Pace et al., reward system in these diverse groups suggests promise as a
2009). The study of altruism and psychopathy has implications therapeutic approach to mitigating violent, destructive behavior.
beyond these traits, as similar brain regions are affected in Post- Approaches involving introspection and promoting acts of
Traumatic Stress Disorder (Keding and Herringa, 2016; Rinne- compassion that activate the reward system, such as mindfulness
Albers et al., 2017). Yoga and controlled eye movement therapies, training, are entering the mainstream of clinical treatment for
called Eye Movement Desensitization and Reprocessing (EMDR), pain management, depression, stress, and behavior modification.
are techniques used for post-traumatic stress (Zepeda Méndez
et al., 2018) and recognized by APA (2017) and United States
Department of Veterans Affairs (2017). This suggests meditative AUTHOR CONTRIBUTIONS
or contemplative practices can affect acquired cognitive traits,
including promoting unselfish behavior. JS and DG contributed equally to the conception, design, writing
of the manuscript, revisions, and approval of the submitted
version.
SUMMARY
Altruism as envisioned by Auguste Comte exists in the general ACKNOWLEDGMENTS
population and in zealous altruists who anchor the benevolence
end of the Selfish–Selfless Spectrum. Advances in genetics, The authors would like to thank Matt Hazzard for contributing
psychology, and neurobiology have increased our understanding the medical illustrations and figures used in this text and Dr.
of social neurocircuitry in the human brain, providing critical Wayne Bell for the encouragement in the study of critical issues
insights into resolving ongoing philosophical, biological, and in neurotheology.

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