AbstractThe 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 that altruistic potential is a common feature in human populations is developed. To go into greater depth in assessing critical features of the social brain, the two extremes of selfish–selfless behavior, callous unemotional psychopaths and zealous altruists who take extreme measures to help others, are compared on behavioral traits, structural/functional neural features, and the relative contributions of genetic inheritance versus acquired cognitive learning to their mindsets. Evidence from population groups ranging from newborns, adopted children, incarcerated juveniles, twins and mindfulness meditators point to the important role of neuroplasticity and the dopaminergic reward systems in forming and reforming neural circuitry in response to personal experience and cultural influences in determining behavior in the selfish–selfless spectrum. The underlying neural circuitry differs between psychopaths and altruists with emotional processing being profoundly muted in psychopaths and significantly enhanced in altruists. But both groups are characterized by the reward system of the brain shaping behavior. Instead of rigid assignment of human nature as being “universally selfish” or “universally good,” both characterizations are partial truths based on the segments of the selfish–selfless spectrum being examined. In addition, individuals and populations can shift in the behavioral spectrum in response to cognitive therapy and social and cultural experience, and approaches such as mindfulness training for introspection and reward-activating compassion are entering the mainstream of clinical care for managing pain, depression, and stress.Keywords: heredity, social, cultural, genetic, neural circuitry, emotions, empathy, compassion
IntroductionIn 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 of others over one’s self-interests. Altruism has since been defined in many senses, including an extreme selflessness in undertaking actions benefiting others without evident self-benefit and incurring personal risk. The conundrum created by Comte’s concept continues to reverberate through social debate, philosophy, theology, and biology, highlighting complex issues in the spectrum of behavior ranging from extreme selfishness to extreme selflessness (Ricard, 2015). The very concept of altruism raises important issues underlying two sharply divergent views of natural social order.Philosophical, political and biological arguments on whether humans are naturally selfish or unselfish have flared for centuries and continue today. Thomas Hobbes contending in his work Leviathan printed in 1651 supporting strong Monarchist governments and running through current culture in Ayn Rand’s popular works assert there is a natural “universal selfishness” manifest in humans, with all behaviors characterized as altruistic being in reality actions that in some measure were in the actor’s best interest. Rand’s continuing influence on political discourse can be seen in the powerful American Speaker of the House and former Vice Presidential candidate Paul Ryan’s attribution of Rand’s Atlas Shrugged as formative in developing his political principles (Weiner, 2012). In Biology, the Oxford University Lecturer and popular science author Richard Dawkins has proclaimed, “We are survival machines – robot vehicles blindly programmed to preserve the selfish molecules known as genes” (Dawkins, 1976).Sharply alternate opinions more supportive of Comte’s vision have also resonated for centuries and continue unabated. Two highly influential 18th century philosophers David Hume and Jean Jacques Rousseau argued that by nature humankind is unselfish. A contention strongly supported today by the prolific neuroscientist and popular science author Richard Davidson (Davidson, 2015). A middle position emphasizing a dual nature for humankind was presented in the 15th century essay by Pico della Mirandola Oration on the Dignity of Man, asserting that we can shape our own destiny by freely choosing whether to descend into brutish behavior or rise to the superior orders of the divine. This is a vision expanded upon by the Dalai Lama who wrote that “the most important thing in this existence of ours is to do something that can be of benefit to others. What we need more than anything is to develop an attitude of altruism – that is really what gives meaning to life” (Dalai Lama, 2007).
The second debate invariably accompanying any discourse on altruistic behavior is what is due to nature versus nurture. To better understand the scientific basis for addressing such profound social and philosophical issues, here we examine the biology and neurological basis of human altruism. We analyze the neural systems and the role of heredity, both genetic and neuron-based (cultural and social), in the development of behavior in the selfish–selfless spectrum, with the goal of discovering how and why portions of the population experience dramatically differing levels of empathy and compassion that strongly influence their worldview and role in society.
Evolution of the Prosocial BrainThe term “altruism” has meant many different things in different times and places. Since Comte’s moral call to place the needs of others above one’s own needs, different disciplines have applied different definitions, and the semantics are themselves a necessary starting point (West et al., 2007). Group selection theory explains behavior such as kin sacrifice in terms of gene survival as opposed to individual survival (Simon et al., 2013; Gardner, 2015). Therefore, according to this evolutionary theory, related individuals will be more likely to perform altruistic acts and decrease their own survival if it benefits the survival of a related individual that carries many of the same genes. This theory is supported by extensive evidence in the literature of preferential treatment of kin (Madsen et al., 2007), while others argue that group selection is an emergent property of natural selection by individual fitness (Zhang et al., 2014; Kennedy et al., 2018). One question is how kin-preference is identified and conferred by an organism. Kin-preference may be a function of the extensive time spent with and proximity to the relative as opposed to an ability to identify genetic relatedness, as argued by cases of cronyism and altruistic preference for close friendships (Stewart-Williams, 2008). From an evolutionary biology perspective, “altruism” or empathic acts could be selected for culturally as a sign of fitness (Taborsky et al., 2016), as attested to by examples of prosocial behavior for non-relatives across the animal kingdom (Field and Leadbeater, 2016; Wilkinson et al., 2016). A more semantically “true” form of altruism may have its roots in the parental instinct to care for offspring, and may explain why empathic behavior is more commonly observed in species with protracted periods of pre-adult growth (Preston, 2013) requiring extended rearing and the resultant passing of learned behaviors, called acquired cognitive learning, as well as “neuron-based heredity,” including social and cultural factors that may have genetic and cognitive elements (Gash and Deane, 2015), to come into play. Thus, the importance of passing to kin the learned behaviors promoting culturally selected traits of compassion may counterbalance the selective value of genes promoting extreme selfish behavior (Bell et al., 2009).The concept of altruism as an enhanced parental instinct relies on the evolution of several factors in both the altruist and the recipient: signaling of kinship status and need for compassion, recognition by kin of the signals, and donation-behavior by the kin (Sinervo et al., 2006). While this behavioral signaling mechanism may underlie parental instinct and compassion which is probabilistically directed toward kin, it is possible that simple parental behaviors – such as offspring retrieval, sustenance and shelter sharing, and emotional comforting – are behavior patterns of signaling-recognition-action that have been enhanced by evolutionary mechanisms (Preston, 2013) resulting in broader altruistic behavior from prosocial brains with greater capacity for receiving and passing on experience and acquired information. And as recent studies have shown, parenting-associated prosocial 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 SpectrumHuman 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 other great apes. The survival and success of large cooperative societies requires most of their members to mute their innate selfish drives and strengthen their selfless behavior. Converging 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. Given the gaps in knowledge in this multidisciplinary area of research, we propose the spectrum be initially plotted as an inverted U-shaped curve with the x-axis representing the range from extreme selfishness to extreme selflessness and the y-axis representing the percent population at each point (Figure Figure11). We also propose that the extreme selfishness end of the spectrum is exemplified by callous-uncaring psychopaths and the extreme selflessness end by zealous altruists that take extreme measures to help others. We hypothesize that the landscape and peak of the curve shifts for given populations based on social and cultural factors (neuronal-based heredity) and genetic makeup....