Abstract

The social brain hypothesis is a useful heuristic for understanding schizophrenia.It focuses attention on the core Bleulerian concept of autistic alienationand is consistent with well-replicated findings of social brain dysfunctionin schizophrenia as well as contemporary theories of human cognitive and brainevolution. The contributions of Heidegger, Merleau-Ponty and Wittgensteinallow us to arrive at a new "philosophy of interpersonal relatedness", whichbetter reflects the "embodied mind" and signifies the end of Cartesian dualisticthinking. In this paper I review the evolution, development and neurobiologyof the social brain - the anatomical and functional substrate for adaptivesocial behaviour and cognition. Functional imaging identifies fronto-temporaland fronto-parietal cortical networks as comprising the social brain, whilethe discovery of "mirror neurons" provides an understanding of social cognitionat a cellular level. Patients with schizophrenia display abnormalities ina wide range of social cognition tasks such as emotion recognition, theoryof mind and affective responsiveness. Furthermore, recent research indicatesthat schizophrenia is a disorder of functional and structural connectivityof social brain networks. These findings lend support to the claim that schizophreniarepresents a costly by-product of social brain evolution in Homo sapiens.Individuals with this disorder find themselves seriously disadvantaged inthe social arena and vulnerable to the stresses of their complex social environments.This state of "disembodiment" and interpersonal alienation is the core phenomenonof schizophrenia and the root cause of intolerable suffering in the livesof those affected.

THE SOCIAL BRAIN

The "social brain" concept originated in the fields of evolutionary biology,primatology and comparative neuroscience, but more recently has become a dominanttheme throughout the cognitive and behavioural sciences. In an influentialpaper, Brothers described "the social brain" as the higher cognitive and affectivesystems in the brain that evolved as a result of increasingly complex socialselective pressures (7). These systemsunderlie our ability to function as highly social animals and provide thesubstrate for intact social cognition, social behaviour and affective responsiveness.

Chance and Mead (8) were among thefirst to suggest that social dynamics might constitute the major driving forcein hominid brain evolution. They stated that "the ascent of man has been duein part to a competition for social position" (8).Chance and Mead's insight was largely overlooked for the next two decades,although a handful of authors such as Jolly (9)and Kummer (10) touched on the themeof social intelligence in their analyses of the social behaviour of lemursand Hamadryas baboons respectively. According to primatologists Byrne andWhiten (11), it was Humphrey's essay"The social function of intellect" (12) that really ushered in the new fieldof study we now term "social cognitive neuroscience". Humphrey argued thatsocial cohesion is fundamental to a context in which the transmission andlearning of skills and knowledge necessary for survival can occur. And socialcohesion within a group depends upon the possession of complex social cognitiveskills by members of that group. Group dynamics are not static - they areoften ambiguous and fluctuate constantly. Thus, in order to survive, groupmembers need to be skilled in the arts of detection, interpretation and calculationof the relative benefits and costs of chosen behaviours.

The skills required to manage social relationships effectively are encompassedin the term "social cognition". Grady and Keightley (13) include the following functions within social cognition:face perception; emotional processing (including both perception of emotionalinformation in the environment and regulation of mood); "theory of mind" (seebelow); and self-reference and working memory. As is common in the cognitiveand behavioural sciences, a range of terminology has emerged in relation tothe concept of social cognition. For example, in relation to apes' capacityto recognize or infer mental states in other individuals, Byrne and Whiten(14) have used the term "metarepresentation".As Brüne (15) puts it, one has"metarepresentations about the social world" and this in turn indicates thepossession of "social metacognition". Drawing on the social machinations ofMachiavelli's Prince, De Waal (16)introduced the term "Machiavellian intelligence" to describe the social andpolitical behaviour of chimpanzees. Others have referred to "mentalizing"(17), "folk psychology" (18) and "the intentional stance" (19).The most familiar term within psychiatry is probably "theory of mind". Thisdescribes the assumption one makes during communication that another individualpossesses a mind just like one's own. Theory of mind is the ability to attributemental states to others and thus forms the very basis of social interactionand communication. Having theory of mind ability enables individuals to engagecognitively in the social arena. Thus it is a core aspect of social cognition.

Social cognitive skills develop in human infants according to a predictablepattern. Contemporary developmental psychologists such as Meltzoff, Gopnickand Trevarthen (20) argue that thechild's sense of "self" and individual consciousness arises from a primaryshared intersubjectivity between mother and infant. In her book "Friday'sfootprint: how society shapes the human mind", social brain pioneer LeslieBrothers (21) discusses the work ofGeorge Herbert Mead, who argued that "meanings... arise in social interaction"and that "self-consciousness arises in the process of social experience. Thegeneralized attitude of others toward oneself becomes linked with the sensationsof one's body, to produce the feelings of personal existence with which weare familiar". Thus, individual consciousness is derived from collective meaningsand, following the Austrian philosopher Ludwig Wittgenstein, words and languageonly have meaning that is derived from the social context of which they area part. If we focus on the development of mature social cognition and theoryof mind ability in normal healthy children, it is generally accepted thatthis is achieved by four years of age (22).Avis and Harris (23) studied Baka pygmychildren in Cameroon and concluded that this is reliable cross-culturally.However, Lillard (24) argues that,in terms of the actual manifestation of theory of mind, cultural variationsdo exist.

With functional imaging modalities such as positron emission tomography,single photon emission computed tomography, and functional magnetic resonanceimaging, we are now able to identify the anatomical and functional neuralbasis for social cognition and theory of mind ability. We can therefore describethe geographical location of the "social brain". It turns out that the anatomyof the social brain is best understood in terms of a network of complex neuralinterconnections linking the prefrontal lobes to the temporal and parietallobes of the brain. These networks are primarily cortical and they principallyconnect frontal and posterior cortical association regions to each other,but there are also vertical links connecting the superficial cortex to deeperand phylogenetically older structures of the brain such as the limbic system.When normal subjects are scanned performing social cognitive tasks (such asviewing facial expressions of emotion, performing theory of mind exercisesor predicting intentions), a number of specific brain regions commonly activate.These include the dorsolateral prefrontal cortex, the orbitofrontal cortex,the anterior cingulate cortex, the amygdala, the superior temporal gyrus,and the parietal association cortex (25-29). The complex comprised of these regionsand their interconnecting neural circuits can be defined "the social brain".

The discovery of so-called "mirror neurons" in the early 1990s providedan understanding of social cognition at a cellular level. First located inBroca's area of the prefrontal cortex in macaques (30),mirror neurons have since been identified in Broca's area, the premotor cortex,the superior temporal sulcus and the posterior parietal cortex in humans (31-33).Mirror neurons activate when the subject observes goal-directed action inanother individual. Thus they serve to mirror or simulate observed intentionalactions within the motor cortex of the observer - they internally "represent"an action (31,34). Other mirror neurons represent stimuli in non-visualmodalities - for example "audiovisual mirror neurons" that activate in responseto auditory signals of intended action (35,36). It has been argued that this mirrorneuron system forms the basis for a "shared manifold" of interpersonal experience(37,38),and it has been proposed that it provides a basis for human empathy (39) or the "experiential understanding ofthe emotions of others" (40). Thus,in the mirror neuron system we have an embedded mechanism for actively engagingin and responding to interpersonal stimuli emanating from the social worldin which we exist. Not surprisingly, this system is located within the anatomicalregion we have termed "the social brain".

SCHIZOPHRENIA AND THE SOCIAL BRAIN

The "social brain" is a useful concept in describing the clinical manifestationsand biological basis of a wide spectrum of psychopathology. There is goodevidence for social brain dysfunction in a variety of mental disorders, bothpsychotic and neurotic in nature. For example, autism has long been conceivedas a social brain disorder (41,42). In my view, this is in part due to thehistorical focus on social dysfunction in autism, while in schizophrenia clinicianshave always tended to become distracted by the more "flamboyant" disturbancessuch as delusions and hallucinations. However, abnormalities of social cognitionand theory of mind ability have also been demonstrated in bipolar disorder(43,44),psychopathy (45) and dementia (46). These findings have led Brüne (47) to assert that the entire spectrum offunctional psychoses, and perhaps all forms of psychopathology, should beregarded as "social brain disorders". However, psychosis, and perhaps classicschizophrenia in particular, represents the "ultimate" or "arch" social braindisorder. In fact, it is in schizophrenia that we encounter a disturbanceof mind that epitomizes dysfunction in every sphere of social cognition andbehaviour.

Constructs of schizophrenia have for a long time been dominated by a focuson symptoms such as auditory hallucinations, delusions and disorganised thoughtsand behaviour. These so-called "positive symptoms", however, are by no meansunique to schizophrenia - most clinicians have encountered all of these disturbancesin patients suffering from mood disorders, dementias, dissociative disordersand substance-related syndromes. Furthermore, within that protean collectionof clinical presentations we consider to be schizophrenia, we encounter significantvariation in "positive" phenomenology. These disconcerting facts have leda number of authors to return to Bleuler's work in an effort to identify thecore characteristic of schizophrenia. Bleuler (48)believed that schizophrenia "is characterised by a specific kind of alterationof thinking and feeling, and of the relations with the outer world that occurnowhere else". Underneath the often obvious but also varied symptoms suchas hallucinations and delusions, there existed, he argued, a less obviousinner unity. He characterized this unity in terms of four "basic symptoms":disturbances of association, ambivalence, affective disturbance, and autism.

Bleuler used the term "autism" to describe detachment from outer realityand immersion in inner life. Minkowski later viewed schizophrenia as a rupturebetween intellect and intuition - the former "associated with analysis andabstract reason" and the latter "based on ... the vitality and temporal dynamismof experience as it is actually lived". This leads to a loss of the "primalsense of vitality or vital connectedness with the world, often accompaniedby a hypertrophy of intellectual tendencies" (48).Sass and Parnas (49) have recentlydescribed two basic schizophrenic phenomena: "diminished self-affection",which is a diminished sense of basic self-presence or "implicit sense of existingas a vital and self-possessed subject of awareness"; and "hyperreflexivity",which is an "exaggerated self-consciousness" that leads to externalised objectificationof the self. Blankenburg's "loss of natural self-evidence" (50) and Kimura's dominance of the "noematic" ("thinking")self over the "noetic" ("existing") self (51)can be considered descriptions of the same process.

If we reflect on Merleau-Ponty's concept of the mind as an "embodied" phenomenon,constructed by and engaged in the physical world of the body and society (5), we can see the way in which all the aboveviewpoints coincide. Schizophrenia represents an alienation from the embodiedself and world: a detachment from Minkowski's "primal sense of vitality";a loss of Blankenburg's "natural self-evidence"; and a detachment from Kimura's"noetic" sense of being an embodied presence in the world. One might thereforeconclude that the weight of 20th century phenomenological efforts to capturethe essential disturbance of schizophrenia supports the idea that the basicproblem faced by these patients relates to their sense of detachment and disembodimentfrom "social self" and "social world".

Several studies have consistently reported abnormalities in a wide rangeof social cognition tasks in schizophrenia. For example, impaired judgementof the direction of eye gaze (52);altered face processing, both in the processing of neutral faces (53) and in the perception of emotional expressions on faces(54,55);and deficits in response and conflict-monitoring (56,57). Theory of mind abnormalities have alsobeen demonstrated in patients using a range of experiments which reveal theirdifficulty in attributing mental states and detecting deception and falsebeliefs (58-60).Brüne (61) argues that these emotionrecognition problems are trait- rather than state-dependent, citing well-replicatedresearch (54,62) which suggests that social cognition problems are enduring"deficits" that characterize the disorder itself. A first episode study byEdwards et al (63) found early manifestationsof emotion recognition deficits, indicating that social brain problems mighteven precede the onset of the disorder.

Structural and functional imaging studies situate social cognition andtheory of mind deficits in schizophrenia within a connected network of prefrontal,temporal and parietal association areas. Structures implicated include thedorsolateral prefrontal cortex (64,65), the orbitofrontal cortex (66), the superior temporal gyrus (65,67), the amygdala (68), the anterior cingulate cortex (57) and the inferior parietal cortex (66,69). Given the roleof the mirror neuron system in social cognition, it is not surprising thatmirror neuron abnormalities are now being detected in schizophrenia (70,71)and this is likely to represent an important domain for future research (72). We may therefore conclude that the primarycognitive deficits in schizophrenia lie within the domain of social cognition,while the primary structural and functional abnormalities are located withinthe distributed cortical networks of the social brain.

Finally, recent research suggests that there are specific abnormalitiesin the structural integrity of the white matter tracts that connect prefrontaland temporo-parietal cortices (73).These findings support the hypothesis that schizophrenia is a disorder offunctional and structural connectivity linking different regions of the cortexto each other and to deeper subcortical structures of the brain (74,75). Since thesenetworks delineate the exact framework of the social brain in humans, I maintainthat this maladaptive disorder can be rightly regarded as a costly by-productof social brain evolution in Homo sapiens. We are a species highly adaptedand attuned to a complex social world. In schizophrenia, we encounter a disorderof this evolved social brain network. Thus, individuals with this diseasefind themselves seriously disadvantaged in the social arena, unable to correctlyread and respond to social signals, and vulnerable to the stresses of theircomplex social environments. This state of "disembodiment" and interpersonalalienation is the core phenomenon of schizophrenia and the root cause of intolerablesuffering in the lives of those affected.

References