The human brain is intrinsically active: it produces electrical and chemical activity both in response to external stimuli and, spontaneously, independently of them. The brain is an autonomously-active motivated neuronal system, genetically equipped with a predisposition to explore the world and to classify what it finds there (Changeux 1985, 2004). On-going spontaneous activity is present throughout the nervous system. In the embryo, spontaneous movements (Narayanan & Hamburger 1971) and waves of endogenous retinal activity (Galli & Maffei 1988; Goodman & Shatz 1993) are thought to play an important role in the epigenesis of neural networks through synapse selection (see below). On-going spontaneous activity is also present in the adult brain, where it is responsible for the highly variable patterns of the electroencephalogram(EEG; Berger 1929; Raichle et al. 2001). Thalamocortical networks generate a variety of oscillations, whose rhythms change across the sleep-wake cycle (Llinas & Paré 1991). Optical imaging methods in anesthetized animals also reveal fast spontaneous states of neuronal activity that, far from being random, exhibit patterns that resemble those evoked by external stimuli. In parallel, functional neuroimaging studies in humans have shown a globally-elevated brain metabolism at rest, with localized patterns suggesting that particular cortical regions are maintained in a high, although variable, state of activity referred to as “default mode” by Raichle et al. (2001).
Hypotheses of knowledge acquisition posit that patterns of spontaneous activity, referred to as “pre-representations”, arise in the brain and are selected by reward signals as “representations” confirmed by both external experience and internal processes of evaluation within a conscious neuronal workspace (Dehaene & Changeux 2011). Such “models of the world” are stabilised through “cognitive games” by analogy with Wittgenstein “language games”, as permanent features of the developing cognitive apparatus, according to a process referred to as “mental Darwinism” (Changeux 2004).
Anticipation of reward signals introduces a delay between the elaboration of tacit plans of action and actual interaction with the world performed by the organism, which presupposes a distinction of temporal states: awareness of the present, remembrance of the past, and anticipation of the future (Barto & Sutton 1982; Schultz et al. 1997; Dehaene & Changeux 2000; Schultz 2006). Without any capacity to evaluate stimuli, the brain could neither learn nor remember: it has to prefer some stimuli to others in order to learn. This classical idea in learning theory has been expressed in neuronal terms by Dehaene & Changeux (1991), and by Edelman in his accounts of primary consciousness (Edelman 1992). In these accounts, learning is a change in actual behaviour, or the storage of a trace subsequently unveiled (Dudai 1989, 2002) through brain categorizations of stimuli. These are given in terms of positive or negative values, understood as something that is taken into account in decision-making and that influences a choice, selection or decision, which can occur on many levels. Through its intense and spontaneous activity, the brain has also been described as a narrative organ, spinning its own neuronal tale (Evers 2009). The narrations will vary greatly between individuals, but each will be self-projective.
The natural egocentricity or individualism of the human brain appears quite pronounced. In its projection of autonomously-produced images, the brain refers all experiences to itself, that is, to its own individual perspective. This self-projection is a biological predisposition that humans possess innately and that is closely connected to our predisposition for developing self-awareness, which Edelman suggests is a necessary condition for developing higher-order consciousness (Edelman 1992; Denton 2006; see also Tulving 1983). The existence of a self-projecting systems monitoring internal processes in the brain was suggested by an early Positron Emission Tomography (PET) study of self-generated actions showing hemodynamic activity in the posterior cingulate cortex (Blakemore et al. 1998). This observation was confirmed and extended by magneto-encephalography following synchronization in the gamma range (55–100 Hz), thus defining a major network of the brain: the paralimbic interaction between the medial prefrontal/anterior cingulate and medial parietal/posterior cingulate cortices and subcortical regions (Lou et al. 2004; rev. Changeux & Lou 2011). Damasio (1999) distinguished a “core consciousness” (core self) from an “extended consciousness” (extended self) that we consider as analogous to the “minimal self” and “extended self” of Gallagher (2000). Minimal self-awareness is prereflexive, immediate and normally reliable, while still involving a sense of ownership of experience (Gallagher 2000). The “extended self” is a coherent self that persists across time and requires a system that can retrieve long-term memories of personal experiences—namely, episodic memory (Gardiner 2001). Consequently, episodic memory retrieval becomes an indispensable component of the more complex forms of self-awareness and consciousness (Tulving 1983).
In the course of growing up, the infant develops the capacity to focus its attention; it learns to distinguish between and recognise objects in its environment, such as faces, and becomes aware of itself as standing in various relations to these objects. Conscious processing develops into auto-distinction (when “this-here” is distinguished from “that-there”). When further developed, the individual becomes aware of itself as a subject of experience and ascribes mental states to itself: auto-distinction evolves into self-awareness (when “this-here” becomes “I”) usually at around one and a half years of age (Lagercrantz 2005), and possibly even earlier (Falck-Ytter et al. 2006; see also Rochat 2001). From the age of six to twelve months, the child typically sees a “sociable playmate” in the mirror's reflection. Self-admiring and embarrassment usually begin at twelve months, and at fourteen to twenty months most children demonstrate avoidance behaviours. Finally, at eighteen months 50% of children recognize the reflection in the mirror as their own and by twenty to twenty-four months this rises to 65%—this is revealed, for instance, by them trying to evince marks on their own nose, taking advantage, in all these instances, of their episodic memory abilities (see Tulving 1983).
An evolved survival function that adds an evaluative element to our brain's self-projective mode of operation is self-interest, expressed as a desire to survive, to be well-fed, safe, to reproduce, and so on. This is not a defining characteristic, for there are exceptions, for example subjects who have a very poorly developed self-interest (Damasio 1994; Damasio & Carvalho 2013). Nor is it necessarily rational, since biological evolution is circumstantial. There is an abundant literature on the phenomenologically rich concept of self-interest in philosophy and ethics, in terms e.g., of enlightenment, egoism, capacity for altruism, etc. Such issues are relevant and interesting but beyond the scope of this discussion. In the present context, self-interest is understood in a minimalistic sense, as an evolved survival function that adds an evaluative element to our brain's self-projective mode of operation.
Self-interest is also a source of the urge to control the immediate environment, and of the need for familiarity, security, and preference for the known. The subjective experience of some level of control and the security that this provides is in fact a necessary condition for the individual to develop in a healthy manner and to consolidate an integrated sense of self (Ledoux 1998). When the external circumstances become severely disturbing, we feel increasingly threatened and have a defence mechanism that is eventually activated: dissociation, here understood as a process whereby information—incoming, stored, or outgoing—is actively prevented from integration with its usual or expected associations.
The human being is, in this sense, a “dissociative animal”: we spend a considerable amount of intellectual and emotional energy on distancing ourselves from a wide range of things that we consciously or non-consciously fear or dislike (Evers 2009). When an experience is too painful to accept, we sometimes deliberately do not accept it; instead of integrating it into our ordinary system of associations, we push it away from us, and prevent it from being integrated into our consciousness. Pushed to an extreme, this tendency may become pathological, e.g., in the development of Dissociative Identity Disorder (cf. DSM-IV), but as a non-pathological process it is an important adaptive function, and a valuable evolutionary asset allowing us to survive events that we would otherwise be unable to endure (Putnam 1989; Evers 2001).
So far, I have described the brain as an autonomously active, self-projective, and selectional neural system with innate evaluative tendencies, e.g., self-interest, control-orientation, and dissociation. These cerebral features characterize the individual, but they are also reflected in the social relationships proper to the human species.
In social animals, self-interest is a source of interest in others. In the case of humans, this social interest focuses primarily on those to whom the self can relate and with whom it identifies, such as the next of kin, the clan, the community, etc. The human brain conjugates opposite tendencies: first, embodied in the human subject, it is engaged in highly individualistic and self-projective actions, such as the search for water or food. But it also mediates co-operative social relationships: the “I” is extended to endorse the group, as a “we”, and distinctions are drawn between “us” and “them” (Ricoeur 1992; Changeux & Ricoeur 2000). Sympathy and aid is typically extended to others in proportion to their closeness to us in terms of biology, e.g., face recognition (Michel et al. 2006; Hills & Lewis 2006), racial out-group versus in-group distinctions (Hart et al. 2000; Phelps et al. 2003), culture, ideology, etc.
Imagining an action or actually performing that action both have similar neural circuits (which include the premotor cortex, supplementary motor area, cerebellum, parietal cortex, and basal ganglia) to those activated when one observes, imitates, or imagines actions performed by other individuals (Jeannerod 2006; Decety 2012). The model mechanism suggested is that actions are coded in terms of perceivable effects (Hommel et al. 2001). Performing a movement leaves a memory of the association between the motor pattern by which it was generated and the sensory effects that it produces. Such stored associations can then be used to retrieve a movement by anticipating its effects. This perception-action coupling mechanism, which includes active sensing and motor-sensory loops (Gordon & Ahissar 2012) and to which may be added the motor theory of language (Liberman & Mattingly 1985), offers a mechanism for intersubjective communication and social understanding by creating functional links between first-person and third-person information (Decety & Sommerville 2003; Jackson & Decety 2004).
Functional Magnetic Resonance Imaging and magneto-encephalography among other methods have led to the demonstration that when children or adults watch other subjects in pain, the neural circuits mobilized by the processing of first-hand experience of pain are activated in the observer (Singer et al. 2004; Cheng et al. 2008). This sharing allows mapping of the perceived affective cues of others onto the behaviours and experiences of the self-oriented response. Decety (2012) argues that, depending on the extent of the overlap in the pain matrix, and complex interactions with personal dispositions, motivation, contextual information, and self-regulation, this can lead to personal distress (i.e., self-centred motivation) or to empathic concern (i.e., an other-oriented response). This basic somatic sensorimotor resonance plays a critical role in the recognition and sharing of others' affective states.
There is an important neural distinction between apprehending and caring that makes it possible to understand the affective state of another without feeling engaged in it. Studies in the neurobiology of empathy (here understood as the ability to apprehend the mental states of others), and sympathy (the ability to care about others) suggest that these abilities involve complex cognitive functions with large individual and contextual variations that depend on both biological and socio-cultural factors (Jackson & Decety 2004; Singer et al. 2004; Singer et al. 2006; Iacoboni et al. 2005; Jackson et al. 2006; Lawrence et al. 2006; Parr & Waller 2006; Engen & Singer 2013). Such results are important, because appreciating the brain’s role in apprehending and responding to the affective states of others can help us understand people who exhibit social cognitive disorders and are deficient in experiencing socially relevant emotions such as sympathy, shame, or guilt.
However, even in supposedly healthy human brains the capacity for other-oriented responses, such as sympathy, is pronouncedly selective and limited by spontaneous aggressive tendencies (Panksepp 1998; Lorenz 1963). When sympathy and mutual aid is extended within a group, they are also (de facto) withheld from those that do not belong to this group. In other words, interest in others is ordinarily expressed positively or negatively towards specific groups—but very rarely are attitudes extended to universal coverage, for example as attitudes towards the entire human species, or towards all sentient beings.
Understanding does not entail compassion, but is frequently combined with emotional dissociation from “the other”. We can easily understand, say, that a child in a distant country probably reacts to hunger or pain in a way that is similar to how children in our own country react to hunger or pain, but that does not mean that we care about those children in equal or even comparable measures. Indeed, if understanding entailed sympathy, the world would be a far more pleasant dwelling place for many of its inhabitants. By nature, we are “empathetic xenophobes” (Evers 2009): we are empathetic by virtue of our intelligence and capacity to apprehend the mental life of a relatively wide range of creatures, but far more sympathetic to the closer group into which are born or choose to join, remaining neutral or hostile to “out-group” individuals.[1]
Thus, in spite of our natural capacity for empathy, sympathy, and mutual assistance, the human being can also be described as a self-interested, control-oriented, dissociative xenophobe. In view of their historic prevalence, it is not unlikely that these features have evolved to become a part of our innate neurobiological identity and that any attempt to construe social structures (rules, conventions, contracts, etc.) opposing this identity must, in order to be realistically implemented, take this biological challenge into account in addition to the historically well-known political, social, and cultural challenges.
A major practical problem is that the effects of our actions are not limited, as are our capacities for engagement. The difficulty of wide involvement due to the brain's self-projective egocentricity is matched by a capacity to cause large-scale effects, which poses serious problems whenever large-scale or long-term solutions are needed—say, to improve the global environment, reduce global poverty, or safeguard future generations. Our societies are importantly construed around egocentric and short-term perspectives—political, economical, etc.—making it extremely difficult to put global or long-term thought and foresight into practice. This is of course only to be expected, since our brains' neuronal architectures are engaged in social interactions and determine the social structures that we can and do develop.
However, our brain identity incorporates social influence. Culture and nature stand in a relationship of mutual causal influence: whilst the organisation of our brains in part determines who we are and what types of societies we develop, our social structures also have a strong impact on the brain’s organisation; notably, they impact upon cultural imprints epigenetically stored in our brains. The genetic control over the brain’s development is subject to epigenetic evolutionary processes; that is to say, to a coordinated and organised neuronal development that is the result of learning and experience and that is intermixed with the action of genes. The door to being epigenetically proactive is, accordingly, opened. In the following analysis of epigenesis by selective stabilisation of synapses I shall discuss the relationship between genotype and brain phenotype; the paradox of non-linear evolution between genome and brain complexity; the selection of cultural circuits in the brain during development; and the genesis and epigenetic transmission of cultural imprints.