Human Becoming: Phylogeny and Ontogeny of Affective Social Behaviour

Human Becoming: Phylogeny and Ontogeny of Affective Social Behaviour

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Human consciousness and uniquely human behavioural distinctives are the end products of a phylogenetic history shared with other hominids, plus a lengthy and uniquely human ontogenetic development. Human behavioural distinctions include the ability to infer abstract causality, abstract theory construction, language embodied in culture, morality, artistic endeavour and spirituality. Our basic thesis here is that human distinctives arise as a result of emotion-based relationships with other persons. A vast literature exists on the necessity of a social setting for the development of language, but other cognitive abilities are also clearly dependent upon early learning which in a human infant necessitates relationship with a caregiver. The development of an embodied spirituality is another human distinctive that can only emerge through nurturant interaction with other persons, both human and the divine. We believe emotion plays a major role in the emergence of these human attributes by providing the valenced states that motivate development of neural circuitry, and this role is especially prominent during early development when the brain is most plastic. The cognitive evolution of the human infant occurred in parallel with the evolution of a uniquely human brain, characterised by an expanded neocortex, extensive lateralization and cytologically unique neurons such as the von Economo or spindle cells, nevertheless, even these specific developments were built on neural adaptations that humans share with other mammals.

Primary emotions

Long term genetic selection has resulted in the existence in vertebrates of basic neural programs providing valenced affective states which prepare and guide responses to appropriate stimuli. In an earlier proposal we suggested (Ellis & Toronchuk, 2005; see also Ellis, 2008b) that primary emotions provide the core nature of the value system guiding the refinement of synaptic connections in interaction with the physical and social environment, hence primary emotions provide the emotional palette that guides brain development. This idea is an elaboration of Panksepp’s formulation of affective neuroscience (Panksepp, 1998, 2001), which describes how neurobiological systems mediate the basic emotions. We suggested that affective neuroscience could be considered a compliment to Edelman’s theory of neural Darwinism (Edelman, 1989, 1992; Edelman & Tononi, 2001), dealing with how brain development and function can be well understood in terms of a process of natural selection acting on neural connections. In the case of “neural Darwinism” the time-course of the selection process referred to is not that of the millennia of phylogeny but rather the developmental course of an individual brain. The term “neural Darwinism” is used in this context to stress the idea of survival during the development of synaptic connections of the strongest, most effective and repeatedly used circuits. Extensive synaptic pruning and apoptosis occur during the early development of each individual brain as excess neural circuits are initially formed and then as individual behaviours are tuned by environmental influence the neurons and synapses which are not of utility do not survive (Kalat, 2007). This means that the basic neural patterns are somewhat “hard-wired” into the developing early brain with the caveat that extensive fine-tuning of neural circuitry takes place predominantly during early stages, but continuing at a declining rate throughout life.

Primary emotional pathways are laid down early and at subcortical limbic and brainstem levels and will tend to be more “hard-wired” than later-forming neocortical pathways and incidentally will be less accessible to conscious awareness. This means that primary emotions, although subject to some fine-tuning by environmental and social stimulation will tend to be more influenced by genetic control and less plastic than cognitive abilities. The primary emotional systems thus come to underlie the later development in the individual of intellectual capacities. Primary emotions also underlie the more behaviourally flexible secondary emotions which arise from blending of primary emotions or interaction with learning. Basic sensory-motor modules involved in pattern-recognition, motor output and problem-solving have access to both the emotional and cognitive systems and are also necessary to enable development of neural circuitry. Through the actions of neurotransmitter, neuromodulator and neurotrophin levels, the wiring of brain circuitry and thereby intellect and self-awareness is widely influenced by the nature, timing and amount of activation in the emotional circuits during early life. Dopamine release in the ventral tegmental pathway is one specific example of how this occurs. The release of brain derived neurotrophic factor (BDNF) as pathways are exercised is another example. According to our synthesis higher brain functions are sculpted on the basis of these primary emotions providing the valenced states that select which neurons, synapses and pathways will survive during subsequent maturation of the brain. It follows that elucidation of the specific nature of these systems is crucial to understanding the way the brain functions and structures itself.

Which emotions are primary?

In a work which virtually inaugurated the discipline of affective neuroscience, Jaak Panksepp described seven “primitive emotional operating systems that exist in limbic and reptilian areas of the brain” (Panksepp, 1998 p.52). He designated these as the SEEKING, RAGE, FEAR, LUST, PANIC (separation distress), CARE, and PLAY systems.1 These are hierarchically organized executive operating systems which give rise to valenced affective states during interaction with several layers of non-specific perceptual, attentional, and cognitive processes. In this view primary emotions are action promoting valenced states with distinct neural circuitry and neurochemistry the consequences of which outlast the precipitating conditions. In contrast reflexive affects such as hunger, pain, and sensory affects such as taste or smell are closely time-locked to their triggering stimuli and are not primary emotions. Panksepp stresses that the differences between primary or prototypical emotions and secondary emotions, such as shame and guilt, include instantiation in more ancient medial and ventral brainstem pathways which are richer in innervation from the viscera and utilize a variety of visceral neuropeptides (Panksepp, 1998, 2003a).

In our view primary emotional systems are those with a long phylogenetic history and they organize complex but flexible reactions by activating or inhibiting autonomic, hormonal and/or somatic changes that were adaptive during evolutionary history. Cosmides and Tooby (2000) also point out that an emotion is a superordinate program which orchestrates and integrates the activities of various functional subprograms, which include reflexive affects, and also subprograms governing perception, cognitive appraisals and feeling states. The specific combination of behavioural components will depend on context and eliciting stimuli.

Basic functioning and survival of the individual

Panksepp’s SEEKING System is the primary task-oriented pathway by which affective goals are met. It is activated on the one hand by primary biological needs characterised by homeostatic signals, but also by signals from other primary and secondary emotional systems and conscious volitional desires. The SEEKING system energizes activity on the basis of a perception of need or dissatisfaction. It is based in the mesolimbic dopamine pathway, but extends to orbitofrontal cortex in humans. It is generalised in its goals able to be activated by any specific need but can also function in a non-specific manner. We have proposed a modification to Panksepp’s view of the SEEKING system on the basis of studies by Berridge (e.g. 2003, 2004) and his colleagues which suggest there are two quite distinct generalised mechanisms involved in reward. One is a motivational, appetitive system (corresponding to SEEKING/expectancy) and the other an hedonic appraisal system linked to consummatory activities and satisfaction. The distinction is illustrated by the fact that addiction involves craving of substances or experiences but not necessarily experiencing satisfaction by them. The wanting and liking components seem to be separate entities. These two systems can be behaviourally dissociated and function independently in rats (reviewed in Cannon & Besikri, 2004) and in humans (Knutson, Fong, Adams, Varner & Hommer, 2001). We suggest therefore the hedonic appraisal component should be considered separately from the SEEKING system and proposed the existence of a separate PLEASURE system in addition to Panksepp’s SEEKING system. This is an important point, but the distinction between the two does not affect the general thesis proposed in this paper.

All organisms must defend themselves against both external and internal threat. In previous papers (Toronchuk & Ellis, 2007 a, b) we argued for the inclusion in the primary emotional systems of a DISGUST system adapted to protect the internal milieu from parasites, pathogens and toxins before any damage is done. This system would have been phylogenetically one of the first affective systems, developing together with PLEASURE and SEEKING in conjunction with development of the immune system’s interaction with the nervous system (c.f. the discussion in Ellis & Toronchuk, 2005). The insula, a primitive cortical area which includes the primary taste area is essential for the disgust response. The wiring of the insula in primates is unique and it has been suggested that the more direct input of primates allowed the later development of increasing conscious self-awareness of the body (Craig, 2003, 2005). A later adaptation with protective advantages utilizing emotional contagion or “resonance” might have promoted the production of the disgust response in individuals following the observation of the same response in conspecifics (Wicker, Keysers, Plailly, Royet, Gallese, & Rizzolatti, 2003). A distinct survival advantage would be conveyed on an individual which avoided a new food after observing a conspecific’s disgust response to that food. The learned acquisition of disgust in children to certain categories of substances may involve preparedness (Rozin & Fallon, 1987), similar to the way in which fear conditioning is easily elicited to spiders, snakes, and angry faces (reviewed in ÷hman & Mineka, 2001). As discussed below this ability to resonate with emotional reactions of others probably gave rise to development of further emotional and cognitive skills that become important in human consciousness and behaviour.

In addition to internal threat there is a need to respond to the dangers created by external threats. In this case, safety is facilitated by the “fight/flight” pair of defence systems: the RAGE system and the FEAR System, engaged when the individual perceives serious threat. Which of the two solutions to threat is implemented in any particular situation is the outcome of an evaluative process based on memories of previous experience and perceptual assessment of the present circumstances. As with DISGUST, some of the same structures activated during the production of fear and anger are also activated during recognition of fear and anger in others utilizing a neural simulation circuitry (discussed further below) which probably contributes later in phylogeny to the development of a theory of mind in others.

Primary emotions of social bonding

The emotional systems promoting social bonding are LUST, PLAY, CARE, PANIC, and we suggest the addition of a POWER or RANK system to Panksepp’s original list. Sexual reproduction, essential for long-term survival of the species is the outcome of the sexual LUST system, clearly an ancient adaptation found in all vertebrates. With the development of mammals there were significant additions to the basic vertebrate social repertoire. Social bonding is however supported by the sexual attraction system and vasopressin and/or oxytocin, hormones involved in sexual behaviour also facilitate pair bonding and are involved in other social behaviours.

According to MacLean (1990, p.247) the basic differences between reptiles and the later evolving mammals are, 1) lactation and maternal care, 2) vocal communication to maintain mother-infant contact, and 3) playful behaviour facilitating social learning. By definition lactation and maternal care are essential for the survival of mammals and these would have been subject to significant selection pressure. Compared with other mammals, hominid infants have a relatively long period of helplessness combined with subsequent need for training in foraging techniques and social behaviours (see Falk, 2004a, Goodall, 1986). This is true of all hominids but two additional factors discussed by Falk contributed to the extended helpless period of human infants. The first was the trend toward a narrow pelvis associated with bipedalism, and the second was the expansion of the human brain. Together these factors would have selected for human infants that were delivered at an increasingly immature stage of development. Because nurture is essential for survival of immature infants, and the infancy of hominids became increasingly extended there must have been selection pressure for establishment of neural circuitry for emotional attachment between mother and infant. This circuitry would be expected to be most highly developed in humans.

In higher animals, social bonding and group cohesion is initially effected primarily by the NEED/ATTACHMENT or Separation Distress System in the young, which triggers panic if there is separation distress, but which also provides satisfaction during closeness. It was necessary for the complementary CARE system , through which parents respond to the young, to evolve in tandem. Panksepp (1998, 2003b) notes that the biological origins of human sadness are rooted in the extended brain system involving the cingulate gyrus that mediates this separation distress in infant animals although this neurological substrate has an even longer evolutionary history in that it was used earlier in phylogeny for perception of physical pain. This is perhaps the reason why humans perceive separation from loved ones as so very similar to pain.

Infant chimps lack the ability to cling to their mothers’ fur in the first two months and so must be supported by the mother on her ventral surface (Plooji, 1984 as discussed in Falk, 2004a). Mothers of older infants use body language and gestural signals to encourage climbing on the mother’s back when it is time to move on. The mother’s use of gestures and facial expressions play a key role in communication with infants and infants develop an intense interest in their mother’s face. Chimp mothers also teach which foods can be eaten and perhaps even tool use (see Falk, 2004a for a review of these behaviours). Chimp infants signal distress to the mother through whisper, hoo and scream vocalizations. Hominid evolution therefore involved tandem evolution of emotional circuitry in adults to provide not merely food, also but emotional nurturance and instruction, and the parallel circuitry in the young to seek and respond to caring adults. This entailed the increasing use of gesture, facial expression, tactile and vocal communication. The increasingly extended period during which hominin young were dependent on caregivers necessitated the development of even more skilled caretaking and the ability of adults to provide instruction. Although the role of these emotions in producing adult human emotional and social behaviour has been well studied, the role of emotion as a selection factor in cognitive development has been less well researched. According to the theory we suggest, mother-infant communication likely provided the emotional motivation for the initial development of language, and its use in adult coalitions was likely a more secondary development.

Learning in human infants has been shown in numerous studies to be critically enabled by reciprocal interaction with the primary care-giver in the early stages of life (e.g. Schore, 1994). The ability for shared attention between infant and mother is critical for the development of a theory of other minds and influences the development of language. Conversely childhood neglect or separation from the caretaker leads to developmental stunting, as for example in hospitalisation syndrome, and appears to be correlated with intellectual and/or social impairment in later life (e.g. Schore, 1994). This phenomenon has been observed in other mammals, but is particularly striking in primates. Thus social emotions provide the valenced state necessary for infant learning, initially taking place in relation to predicting and responding to the actions and emotions of the primary carer.

These systems give rise to the adult need to be part of a social group and tendencies to respond to others in a caring manner. Studies in voles (e.g. Insel & Young, 2001; Lim, Wang, Olazabal, Ren, Terwilliger, & Young, 2004) have identified oxytocin as being implicated both with maternal and adult pair-bonding. That social bonding is supported in part by the more ancient circuitry of the sexual attraction system is suggested in that both vasopressin and/or oxytocin, hormones involved in sexual behaviour, facilitate other forms of social bonding. These systems also facilitate altruistic behaviour in animals, especially social animals such as cetaceans, canids and primates which have relatively well developed memories for social interactions.

Learning, the crucial basis of all higher development, is enabled by the SEEKING system but in young organisms strongly facilitated by the CARE and NEED systems in tandem with the PLAY System. The tendency for young mammals to be involved in play as part of their preparation for both food procurement and adult social roles, suggests that play should also be considered a basic emotional program in the human ancestral lineage and necessary for the normal cognitive development of children. The PLAY system develops significant cortical components in higher mammals parallel with its importance in learning (Bekoff & Byers, 1998; Frost, Wortham & Reifel, 2001). Chimp and bonobo mothers in particular engage in extensive nuzzling, tickling, play-biting, chasing and other forms of play with their infants and play periods are accompanied by facial gestures and vocalizations often including laughter. (reviewed in Falk, 2004a). Panksepp (1998) limits his discussion to “rough and tumble play”, but we believe that in humans the nature of this system has been extended to include more intellectual imaginative play including for example play-acting (Frost et al., 2001) and ultimately allows the development of many aspects of human culture. Lyn, Greenfield and Savage-Rumbaugh (2006) review the use of representational play, in which one object comes to stand for another, in both captive and wild apes.

In mammals, play involves learning social roles and social behaviours (e.g. Bekoff & Byers, 1998; Brosnan, 2006; Keltner, 2006). It is facilitated evolutionarily by the enlargement of the cerebral cortex and the prolonged infant/maternal interaction necessitated by lactation (MacLean, 1990). During play social commitment may be revealed involuntarily and assessed by others. Playful teasing allows the exploring of boundaries. These social aspects may provide one basis for the evolution of altruistic behaviour, and these social aspects also enable enhanced learning. There is a real possibility that optimal cortical plasticity may depend on the activation of play, affection, and other rewards of close attachment. Allowing juvenile rats 30 minutes of rough and tumble play results in increased BDNF transcription in the amygdala and dorsolateral frontal cortex (Gordon et al., 2003). Although much anecdotal information suggests this may also be true in humans the underlying neurophysiological mechanisms are still poorly defined. Play is particularly important in language development (see Paley, 2004; Zigler, Singer & Bishop-Josef, 2004). It is also an essential component of performing arts, ceremonial and celebratory behaviour and an important source of creativity. We speculate that the phylogenetic transition from rough and tumble play alone to the capacity for imaginative play facilitated the development of language through the necessity of understanding and empathising with others that is a critical part of imaginative play.

For many species, group living is crucial for survival advantage, both in terms of finding food and protection against predators as well as in enabling learning. However this inevitably entails a competition for resources that needs regulation to minimize damage to individuals as well as group cohesion. Allocation of rank occurs in animals and humans alike by various competitive processes leading to agonic behaviour that regulates competition in a socially non-destructive way (e.g. de Waal, 1996, Chapter 3; Tomasello & Call, 1997, p.206; Stevens and Price 2002, pp.49-52). Competition takes place in relation to the control of ”territory” regarded in the widest sense, relating not merely to material resources (such as food, material possessions, and geographical areas) but also to social control, sexual mates, status symbols, and intellectual turf. Identity is closely related to territory regarded in this sense. In humans this becomes embodied in social roles and associated status, and underlies many social activities such as competitive sport, and is fundamental in many social arrangements. Thus it becomes a central part of cultural systems. Sewards and Sewards (2003) describe a “power dominance” neural system in mammals which gives rise in humans to subjective feelings of self-esteem, the need to excel, to succeed and to overcome obstacles.

Although Panksepp suggests that social dominance arises during childhood from interactions between the PLAY, FEAR and RAGE systems (1998), we have proposed instead that a genetically determined emotional system concerned with territoriality, dominance and subordination should be added to the list of basic emotions. While ontogenetic development of the individual certainly involves play, we argue for the existence in vertebrate phylogeny of an evolutionarily emotional system more ancient than play on the ground that dominance displays related to territory and access to mates are found in all vertebrate orders and therefore likely predated the PLAY system. It is a very old vertebrate system which functioned to allow competition for mates, territories and other material resources and later gave rise to competition for status and social approval. The striatal complex, which includes the basal ganglia, constitutes a major portion of the “reptilian brain” which is deemed by MacLean to control instinctive, phylogenetically older behavioural patterns. We should note here that the striatal system referred to by MacLean as a “reptilian” component has continued to evolve in mammals playing a major role in motor behaviours. Additional limbic structures including the anterior cingulate gyrus, which plays a role in so many social behaviours, were recruited in mammals for this system. Dominance thus came to involve well developed strategies in hominids who had the intellectual ability for planning and the memory to keep track of subtle interactions and alliances.

The POWER/dominance System is the affective means employed by the evolutionary process to regulate potentially destructive competition for resources by enabling social dominance of some individuals while allowing others to survive and to wait for better opportunities. It involves a desire in humans for higher rank but also an acceptance under normal conditions of assigned status. The associated feelings are pride/high self-esteem in satisfactory circumstances, and shame/low self-esteem when they are unsatisfactory. We propose this ancient system is the precursor to competition for status, need to excel and social approval in humans and relates to Nietzsche’s will to power and Winter’s (1973) implicit power motive.

The POWER system as we propose it involves anterior cingulate cortex (ACC) plus non cortical areas such as peri-aqueductal gray, and hypothalamus (see Sewards & Sewards, 2002; Kroes, Burgdorf , Otto, Panksepp, & Moskal, 2007). Association with the LUST system and competition for mates is indicated by the fact that vasopressin and testosterone are likely involved in its regulation (Thompson, 2006). Furthermore alterations in both vasopressin levels and ACC activity are involved in depression, a disorder that evolutionary psychiatrists see as the human counterpart of social defeat (e.g. Kroes, et al., 2007; Sloman, Gilbert & Hasey, 2003; Stevens & Price, 2002). The development of neocortex in humans allowed for complex integration with cognition resulting in emergence of secondary emotions such as guilt, shame and jealousy. Its malfunctioning can lead to psychiatric disorders the existence of which shed light both on the normal functioning of the system and its evolutionary origins (see Price Gardner & Erickson, 2004; Stevens & Price, 2002, pp. 47-48, 70-73). There is much evidence that low status is a major risk factor for depression in mammals (and even reptiles according to MacLean, 1990), as this probably indexes low probability that a host of needs will be met. We believe this psychiatric data together with observations of animal behaviour, provide evidence that the POWER/dominance system must be recognised as a hardwired system of very ancient origins. Indeed this system involving dominance and submission precedes the evolution of mammals and therefore of the PLAY, NEED and CARING systems, which only reach widespread development in mammals.

Human distinctives

We expect that the human distinctives of theory of mind, language, extensive and creative culture, morality and spirituality all developed in parallel, but language evolution likely played a central role in enabling the emergence of the other attributes. From the following discussion, we infer that these complex developments in humans depend on the existence of several primary emotional systems, which we share with the higher primates and indeed with most mammals. Beings endowed with a single emotional system—merely a feeling of well-being or unhappiness—would not be capable of developing the same range of higher-level repertoires, including moral behaviour. One result of this is that specific psychological or psychiatric problems are likely to arise if specific primary emotional systems are dysfunctional, for whatever reason (as discussed above for depression and POWER). Recognising this feature may be useful in terms of social and medical care. Another result is that the emergence of the full range of human potential depended on the phylogenetic development of emotion-based values.


We believe that the evolutionary development of a theory of other minds was linked specifically to the evolution of the ability to recognize emotions in the self and others. Chimps and bonobos and perhaps some other apes may possess the rudiments of a theory-of-mind as they are able to anticipate the needs and intentions of others and modify their own behaviours accordingly. This has been well documented in the literature for dominance interactions among adults and it is also clearly a part of maternal infant interaction. More significantly, enculturated apes such as the bonobo Kanzi are able to pass linguistically mediated theory-of-mind tests (see Savage-Rumbaugh, Fields, Segerdahl & Rumbaugh, 2005), showing that the neurological prerequisites for theory of mind are available to bonobos. Perhaps ontological development of theory-of-mind requires involvement with caring others who also possess this ability, for example through joint attention which forms during mother infant interactions, and it then becomes socially mediated through linguistic interaction. At any rate ability to be aware of self and others paralleled the development, not of sensory cortex, but of the emotionally salient frontal and limbic cortex.

Interoceptive functions, as well as the experience of disgust (reviewed in Toronchuk & Ellis, 2007a, b), are based on the anterior insula (AI) which in primates possesses an input pathway allowing it (rather than lower structures such as the amygdala and striatopallidum) to become the major focus for valuation of stimuli. The AI and ACC are on one hand architecturally and phylogenetically more primitive than sensory neocortex, but on the other hand , in humans, chimps, bonobos and dolphins they contain aunique recently evolved cellular type (the von Economo (VEN) or spindle neuron described by Nimchinsky, Gilissen, Allman, Perl, Erwin, & Hof, 1999). VENs are hypothesized to be involved in expectancy of behavioural outcomes, human social intuition and formation of a theory of mind. Interestingly self-awareness only arises in humans, great apes, and perhaps some cetaceans i.e. those animals with von Economo neurons. The number of these cells in each species is correlated across both species and age of individuals with degree of self-awareness. Consistent with a proposed role for VENs in self-awareness, humans attain their full compliment of VENs only at about 4 yrs of age.

Core representations of the body arising from structures such as the insula may play a role not only in self-awareness, but also in an “as-if” loop system that allows evaluation and anticipation of events without their actual occurrence. The somatic marker hypothesis (Damasio 1996; Bechara & Damasio, 2005) proposes that the insula provides sensory representation of the state of the body as part of this “as-if” loop mechanism. In support of this, Goldman and Sripada (2005) have proposed that the reading of basic emotions in the faces of others might utilize specialized neural programs, which evaluate emotions of others based on simulation of that state in oneself. During memory this may be accomplished by a reverse simulation which would require the type of “as-if“loop proposed by Damasio. The same “as if” circuitry might function in mirroring the bodily and emotional states of others in the manner in which actions are mirrored by motor neurons in primate brains. As noted above the experience of disgust and its recognition in others activates the AI and ACC (Wicker, et al, 2003). The experience of pain in self and others also activates these areas and response to pain in others is even modulated by the perceived fairness of that person (Singer, Seymour, O’Doherty, Stephan, Dolan, & Frith., 2006) suggesting a neural substrate for empathy. Activation of this region in response to facial expressions of others has been shown recently to correlate with self-reported the ability to empathize with others (Jabbi, Swart, & Keysers, 2007). The functional role of VENs is as yet unknown, but it would be consistent if they were involved in the neural simulations, which make empathy and theory of mind possible.

Damage to the insula and adjacent frontal area produces deficits in moral behaviour, which exist in spite of normal intellectual processing (Damasio, 1996; Koenigs, Young, Adolphs, Tranel, Cushmark, Hauser, & Damasio, 2007). VENs in the frontoinsular and ACC areas are specifically damaged in frontotemporal dementia, a disorder in which emotional and social awareness, empathy and theory of mind are disrupted (Seeley, Carlin, Allman, Macedo, Bush, Miller,.& DeArmond, 2006). Additionally some autistic individuals who have deficits in the theory-of-mind in others have been shown to have dysfunction in these same cells (e.g. Dapretto, Davies, Pfeifer, Scott, Sigman, Bookheimer, & Iacoboni, 2006)

Thus the phylogenetic appearance of VENs is associated with the development of empathy, theory of mind and the ability for moral reasoning. This development might be considered to be a preadaptation influenced by the role of the insula in awareness of bodily state in self and others—a role originally arising from the need to evaluate and avoid contact with and contamination by noxious substances. The brain area originally involved in visceral sensations and evaluating “good taste” and “bad taste” became a necessary component of the neural circuitry for empathy, judging fairness, and making moral decisions. The ACC, which also contains VENs, plays a clear role in the social behaviours of caring, attachment and dominance, emotional behaviours which as described below may also contribute to the evolution of human moral behaviour. The proliferation of von Economo neurons in humans and the expansion of the prefrontal and cingulate cortices likely enabled the progressive development of these features, hence enabling human morality and culture.


The evolution of language ability required not only the evolution of complex conceptual structures, and systems of rules to encode them, but as many have noted (e.g. Fitch, 2000) some motivation to represent and communicate concepts. Why did language develop only in one species? Recent suggestions for the initial selection pressure have stressed adult social interactions such as a Machiavellian motive to outwit group members, gossip as a substitute for grooming (Dunbar, 1996), or the need for males to provide social displays to attract females (e.g. Deacon, 1997, Fitch, 2000) or the perhaps the need to regroup after scavenging. Bickerton (2007) argues against these social theories on the basis of the fact that other primate troops (e.g. baboons) can be very large and complex, but there seemed to have been no selection pressure for other primates to develop anything approaching protolanguage. In our view, all of the above mentioned possible selection pressures involve adult activities while our thesis, in contrast, is that the emotional relationship between infant and carer provides the first instance, both in phylogeny and in ontogeny, of social motivation for language development. This is because of the primary importance of infant care in the lives of hominids coupled with the incredible post-natal growth that the brain of infants, in particular human infants, undergoes. Cortical circuits are primarily set up in this post-natal period. Play relationships with other juveniles during the increasingly long period of hominin childhood provide increasing opportunities for learning to communicate with others during the period when the brain is still undergoing maturation. Indeed, that the prefrontal area of humans requires twenty years to reach full maturation.

The relative ease with which children develop language suggests a relation between the structure of language and its acquisition. This led to Chomsky’s proposal of the existence of a Universal Grammar. One possible explanation for the appearance in all human lineages of a universal grammar is that special brain mechanisms slowly evolved to support language (the “continuity” theory e.g. Corballis, 2003; Dunbar, 1996; Falk, 2004a, b; Pinker & Bloom, 1990). A second theory is that brain mechanisms supporting language appeared suddenly perhaps due to a small number of mutations (the “discontinuity” theory e.g. Bickerton, 2007). The discovery of a role of the FOXP2 gene in language (Lai, Gerrelli, Monaco, Fisher, & Copp, 2003) spurred a great deal of initial excitation for those in the latter camp. A variation of this theme that language is the result of a faculty unique to humans is held by Fitch, Hauser and Chomsky (2005) who see the essential features of language as exaptations from other abilities. Another possibility suggested by Christiansen and Chater (2008) is that rather than the brain adapting to support language providing a neural basis for universal grammar, language itself was the subject of selection pressure. Language was selected for ease of learning by hominins who already had particular neural substrates. Because language adaptation is culturally based, changes in language due to cultural evolution occur much faster than biological changes in the brain. One might expect that any so-called “language genes” that appeared in a population would diverge especially rapidly, as early humans spread out geographically, leaving the question of how an original universal grammar remained universal. Therefore, it is more likely as Christiansen and Chater suggest that language evolved to fit pre-existing structures of the brain rather than the other way around, and language was adapted to use a general purpose rather than a specialized modular strategy.

The structures that were available for the use of language were the limbic structures used by primates in vocalization, in particular the ACC, as well as the motor structures used in gesturing. It has been suggested (e.g. Arbib, 2005; Corballis, 2003) that because the analogue of Broca’s area in the monkey contains mirror neurons responsive to gestures in other individuals, language arose through gradual adaptation of the gestural system. Bonobos use gestures in a flexible manner in communication with conspecifics adjusting for the attentional state of the recipient (Pika, Liebal & Tomasello, 2005). Subadults are the most common users of gestures and social learning appears to be responsible for acquisition of at least some specific gestures. In connection with the gestural theory we think it is interesting to note that VENs, probably involved in mirroring emotions, are predominantly on the right side of the brain–the side activated by emotion in other people. Prosody, and presumably early motherese, also activate the right side. Broca’s area, which contains mirror neurons in both monkeys and humans, overlaps this area, but is on the left side. This suggests that brain lateralization proceeded such that one side came to mirror emotions and the same area on the other side to mirror gesture and voluntary vocalizations.

It is usually asserted that non-human primate vocalizations are involuntary because they arise from limbic rather than neocortical areas whereas human speech is under the voluntary control of a motor area, namely Broca’s area (this anatomy is discussed in Ploog, 2003).Captive common chimpanzees, however, have been shown to use vocalization in a voluntary manner, not associated with emotional outburst, to direct attention of onlookers (Hopkins, Taglialatela & Leavens, 2007). Gaining attention from others is then in these chimps both voluntary and a socially motivated behaviour. The enculturated bonobo Kanzi’s use of spoken English (Taglialatela, Savager-Rumbaugh & Baker, 2003) indicates that it is neurologically possible for bonobos to vocalize voluntarily. Perhaps the cingulate gyrus which initiates vocalization in monkeys provides the emotional flavour in bonobos for voluntary vocalization through its known connections with motor areas.

Even chimp mothers and infants take turns during play (reviewed in Falk 2004a) perhaps providing a basis for the development in protomotherese of a more voluntary action than that assumed for typical primate vocalizations. Kanzi has been shown to engage in the type of communicative turn taking that suggests a pattern of human discourse even though the individual segments of discourse are very short and devoid of complex syntax (Benson & Greaves, 2005). Analysis of his discourse with trusted caretakers suggests that he is indeed well aware of the communicative uses of discourse with vocal and gestural components. The way in which Kanzi and his kin learned language, however, was quite different from previous attempts at teaching language to apes. These bonobos have been exposed to language early in life in a manner approximating that of human children within a family setting. They have clear emotional ties to their human caregivers and exist as part of a unique Pan/Homo culture (Savage-Rumbaugh, Fields & Spircu, 2004). The relationship has not been merely social, it is social with strong emotional ties, attachment and nurture. Some of the videos of caregivers interacting with Kanzi2 suggest that they use language with inflections and vocal stress similar to motherese. The nurturing atmosphere and “family” like upbringing may in fact be the key to ape language learning.

Modern human motherese uses exaggerated vowels, hyperarticulation, heightened prosody, and exaggerated facial expressions all of which contribute to emotion regulation in infants. Human infants in turn are predisposed to respond to motherese which then prepares the infant to be attuned to the phonetic and semantic aspects of their native language. Motherese also maintains joint attention and encourages infants to learn turn taking aspects of dialogue (reviewed in Falk, 2004a). The emotional aspects of motherese cause it to be so attractive to infants, but the end result is that the emotional motivation leads to the ontological process of learning phonological and semantic aspects of language. Other modern hominids do not vocalize nearly as much with infants, but the evolutionary trend toward lengthened childhood, immature infants and increasing brain size were likely coupled with an increased selection pressure for more complex nurturing of infants which in turn led to increasing joint attention, understanding of other minds, and use of communicative gestures and sounds.

Non-vocal sounds such as lip smacking, used by chimps were likely abundant in early motherese. Neither clicks nor whispers require descent of the larynx into the position necessary for human speech. Even though we do not know when the larynx of hominins descended (Fitch, 2000), clicks and whispers could have been used at the earliest stages. Indeed some linguists think the first human language might have been the proto click-language, from which the Khoisan family originated (e.g., Pennisi, 2004). The production of clicks was certainly physiologically possible for early hominins.

The voluntary use of nonsense sounds in mother-infant play would be motivated by the social emotion of CARE and PLAY, but freed from the more immediate and reflexive nature of e.g. alarm calls. Representational play and chasing may have been extended at that point to include actions feigning intentions such as “I’m going to get you”, but these were freed from aggressive intent. As sounds also began to be used in play, siblings might begin to use in common some of the same sounds used by their mother, and also use these sounds in play with other unrelated juveniles. In this manner local cultures of sound use might develop. Rather than the development of a universal protolanguage, it would be enough for further evolution of language that some individuals learned to use sounds or gestures generally to represent concepts. Over long periods of time, local cultures of juveniles may then have developed their own proto-dialects though cultural learning but motivated by social play. The concept that one thing can stand for another would have been the necessary development which emerged in part from representational and feigning play.

Our view is similar to that of Falk (2004a, b) in that we stress mother-infant interaction and the use of motherese, except we are less convinced that the original selection pressure for motherese was for soothing infants because foraging hominin mothers began to engage in “putting the baby down” (the label she has given her theory to free their hands for foraging tasks. Rather we think the selection pressure over the increasingly long period of infant and juvenile dependency was more general and included mutual attraction, play and instruction, and did not necessarily depend on any particular baby-carrying strategy.. Proto-motherese and proto-language likely had multimodal origins in a structureless combination of gesture, facial expression, gaze, vocal and non-vocal sounds. In addition other emotional needs such as those involved in mating and social grooming probably worked concurrently to provide multiple selection pressures on the use of protolanguage. It is probably significant that Broca’s area and its primate analogue contain mirror neurons for both hand and facial movements and this probably lead to the use of both types of signals concurrently. Over time, protolanguage would come to rely more heavily on the vocal mode although modern speech is still strongly connected to gesture.

Admittedly there remain some problems with any continualist theory, including ours. If protolanguage was holistic with strings of utterance rather than employing short discrete units, a mechanism is needed to segment longer utterances into meaningful individual units (words). The fractionation of longer holistic strings into short segments might be an intellectually more difficult task than learning individual words as symbols (see Tallerman, 2007 for discussion). This presents a problem for the theory that language evolved from holistic protolanguage. However even the use of a very few short sounds may have led to the realization that sounds may be representational. The evidence for representational play in chimps, and pretense in captive bonobos, indicates that this ability was available to early hominins as well. We believe the holistic (top-down) approach to language development (based in its use to convey meaningful statements as a whole to the recipients) is likely to be the right one (see e.g. Krashen and Terrell 1983), even if the details of how it works out are still obscure.

Another problem that might be raised is how a fully developed syntax could emerge from protolanguage consisting of something like the telegraphic speech used by modern two year olds. The evolution of the ability to represent recursion is viewed by most as a necessary component of the evolution of language (Fitch, Hauser & Chomsky, 2005). Recent experiments in which starlings were able to discriminate syntactic patterns (Gentner, Fenn, Margoliash & Nusbaum, 2006), however, suggest that perhaps rudimentary recursion is not an exclusively human ability. In addition there is perhaps one modern language, Piraha, which lacks the use of recursion, as well as colour names, numeracy, and past and future tenses (Everett, 2005; 2007a, b) and this case has been used to challenge Chomsky’s model of universal grammar. Of course, the case of Piraha does not tell us whether recursion is necessary for language to evolve, as its loss in this group may be a secondary development. A recent hypothesis put forward by Okanoya (2007) is that the unique components necessary for language, in particular recursion, emerged from interactions among more general preadaptations for emotion, sensory motor-integration, and a mirror system of imitation. A further consideration of the evolution of syntax is beyond the scope of this paper (see Tomasello 2003 for the probable mode of resolution). Our hypothesis is that language emerged along with culture from pre-adaptations of emotional systems, with childhood socialization playing a major role.


At present, an extensive debate exists around the extent to which innate mental modules influences human moral behaviour. Some biologists such as Marc Hauser (2006) propose the existence of dedicated moral modules similar to Chomsky’s language modules. However, in light of the fact that it is now agreed that several emotions seem to contribute to moral behaviour, the idea of a dedicated moral module is questionable. As with the evolution of language, it is difficult to see how all the various preadaptations would come together into one genetically controlled module. Jonathan Haidt has in contrast proposed the existence of several evolutionarily prepared moral domains each of which offers survival benefits in a social setting and which act somewhat independently. These include 1) altruism and kinship ties 2) reciprocity, and concern for fairness 3) rank and authority 4) in-group loyalty, and 5) moral purity and avoidance of contamination (Haidt & Joseph, 2007).

According to our view (Toronchuk & Ellis, 2007c), each of the emotional operating systems has the potential to either overtly or subliminally influence behaviour thereby providing motivational force for Haidt’s suggested moral domains. These emotional operating systems are part of the human biological heritage and influence the content of our moral behaviours. Because each emotional system has been moulded by unique selection pressures and uses distinctive neural circuitry the influence each has on moral intuition remains separate and independent of the influence of other emotions. For example, a recent study by Sherman, Haidt and Coan (n.d.) suggests indeed that attitudes of anger and disgust influence moral decision making separately.

The emotional systems that have been adapted to function during social encounters play obvious roles. We expect that the primary emotional POWER system influences both the authority/subordination domain described by Haidt and the domain giving rise to reciprocity/ fairness/concern for justice. In addition, the CARE nurturance system of adults plays an obvious role in moral intuitions and together with the separation distress (PANIC) system has been adapted to support various forms of altruistic behaviour. The reciprocity and fairness domain of Haidt may derive in part from the PLAY system, which promotes learning of appropriate social behaviours in juveniles (see Bekoff & Byers, 1998; Brosnan, 2006; Keltner, 2006). Falk (2004a) discusses the way chimp mothers and infants engage in turn taking during play. The RAGE system probably also influences reciprocity by rousing the desire to punish cheaters who violate conditions of reciprocity.

In our proposal of DISGUST as a primary emotional system, we suggested that while disgust originally regulated ingestive and tactile behaviours, these mechanisms were then further developed to form a primary emotional system that allows evaluation of reinforcers and motivates avoidance. Rozin, and Haidt (Rozin & Fallon, 1987; Haidt, Rozin, et al., 1997) noted that disgust is more than avoiding bad taste; it hinges on avoidance of contamination. However, they see only human disgust as contamination related, whereas we suggest that the theme of disease avoidance has ancient origins (Toronchuk & Ellis, 2007a, b). A survey (Curtis, et al., 2004) showing that disease-salient contact stimuli such as bodily secretions, viscous substances, vermin and sick or dirty people universally elicit disgust supports this contamination-avoidance origin. Our proposal is that there is an evolutionary trajectory from illness-related reactions, through learned aversions and avoidance responses, to human core disgust and eventually to a secondary emotion encompassing socio-moral attributes. Nutritional-, sexual-, and socially-related stimuli plus ideational components are all able to activate the SEEKING (approach) or DISGUST (avoidance) systems in analogous ways. Not only do animals avoid foods which have been paired in the past with illness (reviewed in Toronchuk & Ellis, 2007a) but it has been shown that rats will even avoid copulation after it has been paired with illness (Peters, 1983). This suggests an underlying similarity between conditioned taste disgusts and social disgust.

Schaller has proposed what he calls an “emotional immune system” based on an evolutionary bias to avoid others who might be diseased, but which may extend to other areas of social avoidance, cultural attitudes and religious rituals (Schaller & Duncan, 2007). Humans avoid others with obvious disease but also any difference from the norm—including asymmetries, disabilities and obesity—because difference from the norm may signal underlying ill health or poor genetic potential. Foreigners are also more likely to carry pathogens for which we have no immunity. Schaller’s theory thus bridges the disease- avoidance function of disgust with emotional prohibitions concerning touch and sexual contact with others. Morals are biologically biased to consist of rules for sexual contact and social proximity to avoid biological contamination. The main point is that both moral purity and in-group loyalty have a phylogenetic history in a basic emotional system, which comes to influence human culture in dramatic ways.

Human culture

Although culture has been shown to exist in animals the explosion of human creativity that seemed to occur only within the last 100,000 years was likely linked to language evolution. Human imagination artistic endeavours, and various aspects of culture, we suggest, have roots in the emotional programming of young mammals, and primates in particular, to engage in play behaviours with conspecifics, a behaviour which functions to underpin learning and preparation for adult life.

The expanded human brain, extended childhood, and cultural scaffolding provided during childhood by older individuals are all necessary for the development of human nature. Kanzi and other enculturated apes are high achievers precisely because they have been provided with the cognitive scaffolding of their human caretakers (see e.g. Savage-Rumbaugh et al., 2004, 2005; Segerdahl, Fields & Savage-Rumbaugh, 2005). Their unique language, imitation of intentional actions and toolmaking abilities would not have emerged without emotional involvement and shared attention with humans, which enabled learning of behaviours that they did not invent themselves. Furthermore culture is a progressive process as those who have lived and worked with these apes note that the young born to already enculturated bonobos “gaze, think, gesture and behave in nonverbal ways that increasingly diverge” from non-enculturated bonobos (Savage-Rumbaugh, et al., 2005). Although even wild apes engage in representational play, only those bonobos with acquired linguistic ability engage in play which involves true pretense (Lyn et al., 2006) showing that not only does cultural scaffolding further language use, but language also furthers cultural development As Savage-Rumbaugh and colleagues (2005) eloquently note “We are forced to acknowledge that skills we have assumed to be fundamental to all aspects of human cognition (i.e. language, imitation and ‘theory of mind’) are not innate. They emerge within a cultural environment that has been constructed of whole cloth across millennia of social weaving. Whether we approve or not, we are products of the very cultures we ourselves have, in co-constructed dialogic exchanges, brought into being.”

We believe the peculiar inabilities of feral children suggest that it is difficult even for human children to participate in human culture if pre-existing social and emotional framework is not available to them at a very early age. Another suggestion for the importance of pre-existing culture may exist in the curious inabilities of the Piraha people of the Amazon jungle to learn numeracy, as well as their lack of colour terms, recursive language and relative tenses (Everett 2005, 2007a, b). If the anthropologist Everett, who lived with the Piraha for many years, is correct in placing these verbal abilities within cultural processes, it suggests that the type of scaffolding necessary to develop grammar entails certain kinds of social interactions. In Everett’s words, “Piraha culture constrains communication to nonabstract subjects which fall within the immediate experience of interlocutors”. They have no myths, fiction, drawing or art. This suggests to us that in this case there may exist a culture which provides no emotional motivation to develop a more complex language or other cultural endeavours and nothing on which to scaffold development of such in its children.

We think the scaffolding necessary for the phylogenetic and ontogenetic emergence of human language, culture, morality and spirituality, necessarily entails identification with enculturated others and this identification has an emotional basis fostered in early childhood. It is provided by the mirror neuron system and the development of empathy and theory of other minds. Only through interaction with other humans, a process that necessarily engages affective systems, can these human distinctives develop in the maturing human child. Thus, human minds cannot be understood on their own (Donald, 2001); they develop to be what they are through social interaction during the developmental process. This emergence is a form of top-down action from society to the individuals who comprise it (Ellis 2008a).


The complex awareness of self and others fostered by normal human society allows the emergence in human consciousness of the apprehension of transcendent reality. In spite of our highly developed emotional and cognitive capacities, however, there are no assured mechanisms for either moral behaviour or self-transcendence. The human condition seems to entail inevitable internal conflict as indeed many religious traditions suggest. Given our conflicting tendencies for both dominance and nurturance, it is unclear how universal morality and kenotic love can come about without some form of self-transcendence assisted by religious or spiritual experiences of various kinds. Nancey Murphy (1998) states “The person is a physical organism whose complex functioning both in society and in relation to God gives rise to “higher” human capacities such as morality and spirituality.” Indeed, it is through interaction with others that personhood is called forth in human infants and developed in adults. The development of an embodied spirituality accompanied by telos and meaning is a human distinctive that can only emerge in nurturant interaction with other persons, human and divine.



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1 We follow Panksepp’s use of capital letters to differentiate these as operating systems rather than emotional feelings per se.

2 We thank James Benson and William Greaves of York University for video footage of Kanzi and helpful discussion.