The social brain hypothesis of schizophrenia

Abstract

The social brain hypothesis is a useful heuristic for understanding schizophrenia. It focuses attention on the core Bleulerian concept of autistic alienation and is consistent with well-replicated findings of social brain dysfunction in schizophrenia as well as contemporary theories of human cognitive and brain evolution. The contributions of Heidegger, Merleau-Ponty and Wittgenstein allow us to arrive at a new "philosophy of interpersonal relatedness", which better reflects the "embodied mind" and signifies the end of Cartesian dualistic thinking. In this paper I review the evolution, development and neurobiology of the social brain - the anatomical and functional substrate for adaptive social behaviour and cognition. Functional imaging identifies fronto-temporal and fronto-parietal cortical networks as comprising the social brain, while the discovery of "mirror neurons" provides an understanding of social cognition at a cellular level. Patients with schizophrenia display abnormalities in a wide range of social cognition tasks such as emotion recognition, theory of mind and affective responsiveness. Furthermore, recent research indicates that schizophrenia is a disorder of functional and structural connectivity of social brain networks. These findings lend support to the claim that schizophrenia represents a costly by-product of social brain evolution in Homo sapiens. Individuals with this disorder find themselves seriously disadvantaged in the social arena and vulnerable to the stresses of their complex social environments. This state of "disembodiment" and interpersonal alienation is the core phenomenon of schizophrenia and the root cause of intolerable suffering in the lives of those affected.

For more than a century we have witnessed within psychiatry the emergence of numerous explanatory models or hypotheses of schizophrenia. In this article I introduce the concept of an evolved social brain in Homo sapiens that is vulnerable to developmental disturbances, which manifest as psychopathologies such as psychosis. This social brain hypothesis is a useful heuristic for understanding schizophrenia, since it accommodates existing models of the disorder and in addition focuses our attention on perhaps the most devastating and consistently reported symptoms: the loss of social cognitive skills and the alienation of the self from the social world.

Furthermore, the social brain hypothesis is consistent with contemporary theories of human cognitive and brain evolution, individual cognitive, emotional and social development, and the anatomical and physiological structure and function of neural networks underlying complex social cognition and behaviour. Finally, this hypothesis reflects the recent change in the philosophical approach to the mind/brain issue (1,2).

Most contemporary philosophers and phenomenologists of mind have abandoned the Cartesian model of an isolated ethereal mind separated from body and environment, in favour of a physically and socially integrated construct of mind, embodied in the living world. For 400 years Rene Descartes' dualistic model dominated thinking within the biological and social sciences (3) and its pervasive influence is evident in the "mind-body split" that characterises our modern construct of mental life. In recent decades, and in response to the obvious failures of Cartesianism, philosophers such as Martin Heidegger (4) and Maurice Merleau-Ponty (5) have developed a new philosophical basis for the study and understanding of human behavioural and mental phenomena - a philosophy that reflects the interpersonal nature of mental life. According to Bracken (6), Heidegger describes the world as existing "a priori", i.e. before our human representation of it as thought. Bracken explains: "Existence, in the sense of lived human existence, involved and embedded in the world, is the necessary precedent and the enabling condition of thought" (6). In his famous "The phenomenology of perception", Merleau-Ponty (5) wrote of the human condition as fundamentally "being-in-the-world"; the mind exists as an "embodied" phenomenon, constructed by and engaged in the physical world of the body and society. These great thinkers (and their successors) have provided us with "a powerful antidote to the dominance of Cartesianism in the humanities and the human sciences" (6) - a new "philosophy of interpersonal relatedness" that resonates strongly with state-of-the-art research findings in the cognitive, developmental and evolutionary neurosciences.

THE SOCIAL BRAIN

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

Chance and Mead (8) were among the first to suggest that social dynamics might constitute the major driving force in hominid brain evolution. They stated that "the ascent of man has been due in 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 theme of social intelligence in their analyses of the social behaviour of lemurs and Hamadryas baboons respectively. According to primatologists Byrne and Whiten (11), it was Humphrey's essay "The social function of intellect" (12) that really ushered in the new field of study we now term "social cognitive neuroscience". Humphrey argued that social cohesion is fundamental to a context in which the transmission and learning of skills and knowledge necessary for survival can occur. And social cohesion within a group depends upon the possession of complex social cognitive skills by members of that group. Group dynamics are not static - they are often ambiguous and fluctuate constantly. Thus, in order to survive, group members need to be skilled in the arts of detection, interpretation and calculation of the relative benefits and costs of chosen behaviours.

The skills required to manage social relationships effectively are encompassed in the term "social cognition". Grady and Keightley (13) include the following functions within social cognition: face perception; emotional processing (including both perception of emotional information in the environment and regulation of mood); "theory of mind" (see below); and self-reference and working memory. As is common in the cognitive and behavioural sciences, a range of terminology has emerged in relation to the concept of social cognition. For example, in relation to apes' capacity to 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 the possession of "social metacognition". Drawing on the social machinations of Machiavelli's Prince, De Waal (16) introduced the term "Machiavellian intelligence" to describe the social and political 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". This describes the assumption one makes during communication that another individual possesses a mind just like one's own. Theory of mind is the ability to attribute mental states to others and thus forms the very basis of social interaction and communication. Having theory of mind ability enables individuals to engage cognitively in the social arena. Thus it is a core aspect of social cognition.

Social cognitive skills develop in human infants according to a predictable pattern. Contemporary developmental psychologists such as Meltzoff, Gopnick and Trevarthen (20) argue that the child's sense of "self" and individual consciousness arises from a primary shared intersubjectivity between mother and infant. In her book "Friday's footprint: how society shapes the human mind", social brain pioneer Leslie Brothers (21) discusses the work of George Herbert Mead, who argued that "meanings... arise in social interaction" and that "self-consciousness arises in the process of social experience. The generalized attitude of others toward oneself becomes linked with the sensations of one's body, to produce the feelings of personal existence with which we are familiar". Thus, individual consciousness is derived from collective meanings and, following the Austrian philosopher Ludwig Wittgenstein, words and language only have meaning that is derived from the social context of which they are a part. If we focus on the development of mature social cognition and theory of mind ability in normal healthy children, it is generally accepted that this is achieved by four years of age (22). Avis and Harris (23) studied Baka pygmy children 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 variations do exist.

With functional imaging modalities such as positron emission tomography, single photon emission computed tomography, and functional magnetic resonance imaging, we are now able to identify the anatomical and functional neural basis for social cognition and theory of mind ability. We can therefore describe the geographical location of the "social brain". It turns out that the anatomy of the social brain is best understood in terms of a network of complex neural interconnections linking the prefrontal lobes to the temporal and parietal lobes of the brain. These networks are primarily cortical and they principally connect frontal and posterior cortical association regions to each other, but there are also vertical links connecting the superficial cortex to deeper and phylogenetically older structures of the brain such as the limbic system. When normal subjects are scanned performing social cognitive tasks (such as viewing facial expressions of emotion, performing theory of mind exercises or 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 regions and their interconnecting neural circuits can be defined "the social brain".

The discovery of so-called "mirror neurons" in the early 1990s provided an understanding of social cognition at a cellular level. First located in Broca'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 in another individual. Thus they serve to mirror or simulate observed intentional actions within the motor cortex of the observer - they internally "represent" an action (31,34). Other mirror neurons represent stimuli in non-visual modalities - for example "audiovisual mirror neurons" that activate in response to auditory signals of intended action (35,36). It has been argued that this mirror neuron 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 of the emotions of others" (40). Thus, in the mirror neuron system we have an embedded mechanism for actively engaging in and responding to interpersonal stimuli emanating from the social world in which we exist. Not surprisingly, this system is located within the anatomical region we have termed "the social brain".

SCHIZOPHRENIA AND THE SOCIAL BRAIN

The "social brain" is a useful concept in describing the clinical manifestations and biological basis of a wide spectrum of psychopathology. There is good evidence for social brain dysfunction in a variety of mental disorders, both psychotic and neurotic in nature. For example, autism has long been conceived as a social brain disorder (41,42). In my view, this is in part due to the historical focus on social dysfunction in autism, while in schizophrenia clinicians have always tended to become distracted by the more "flamboyant" disturbances such as delusions and hallucinations. However, abnormalities of social cognition and 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 of functional psychoses, and perhaps all forms of psychopathology, should be regarded as "social brain disorders". However, psychosis, and perhaps classic schizophrenia in particular, represents the "ultimate" or "arch" social brain disorder. In fact, it is in schizophrenia that we encounter a disturbance of mind that epitomizes dysfunction in every sphere of social cognition and behaviour.

Constructs of schizophrenia have for a long time been dominated by a focus on symptoms such as auditory hallucinations, delusions and disorganised thoughts and behaviour. These so-called "positive symptoms", however, are by no means unique to schizophrenia - most clinicians have encountered all of these disturbances in patients suffering from mood disorders, dementias, dissociative disorders and substance-related syndromes. Furthermore, within that protean collection of clinical presentations we consider to be schizophrenia, we encounter significant variation in "positive" phenomenology. These disconcerting facts have led a number of authors to return to Bleuler's work in an effort to identify the core characteristic of schizophrenia. Bleuler (48) believed that schizophrenia "is characterised by a specific kind of alteration of thinking and feeling, and of the relations with the outer world that occur nowhere else". Underneath the often obvious but also varied symptoms such as hallucinations and delusions, there existed, he argued, a less obvious inner 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 reality and immersion in inner life. Minkowski later viewed schizophrenia as a rupture between intellect and intuition - the former "associated with analysis and abstract reason" and the latter "based on ... the vitality and temporal dynamism of experience as it is actually lived". This leads to a loss of the "primal sense of vitality or vital connectedness with the world, often accompanied by a hypertrophy of intellectual tendencies" (48). Sass and Parnas (49) have recently described two basic schizophrenic phenomena: "diminished self-affection", which is a diminished sense of basic self-presence or "implicit sense of existing as a vital and self-possessed subject of awareness"; and "hyperreflexivity", which is an "exaggerated self-consciousness" that leads to externalised objectification of 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 above viewpoints coincide. Schizophrenia represents an alienation from the embodied self 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 therefore conclude that the weight of 20th century phenomenological efforts to capture the essential disturbance of schizophrenia supports the idea that the basic problem faced by these patients relates to their sense of detachment and disembodiment from "social self" and "social world".

Several studies have consistently reported abnormalities in a wide range of social cognition tasks in schizophrenia. For example, impaired judgement of 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 also been demonstrated in patients using a range of experiments which reveal their difficulty in attributing mental states and detecting deception and false beliefs (58-60). Brüne (61) argues that these emotion recognition problems are trait- rather than state-dependent, citing well-replicated research (54,62) which suggests that social cognition problems are enduring "deficits" that characterize the disorder itself. A first episode study by Edwards et al (63) found early manifestations of emotion recognition deficits, indicating that social brain problems might even precede the onset of the disorder.

Structural and functional imaging studies situate social cognition and theory of mind deficits in schizophrenia within a connected network of prefrontal, temporal and parietal association areas. Structures implicated include the dorsolateral 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 role of the mirror neuron system in social cognition, it is not surprising that mirror 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 primary cognitive deficits in schizophrenia lie within the domain of social cognition, while the primary structural and functional abnormalities are located within the distributed cortical networks of the social brain.

Finally, recent research suggests that there are specific abnormalities in the structural integrity of the white matter tracts that connect prefrontal and temporo-parietal cortices (73). These findings support the hypothesis that schizophrenia is a disorder of functional and structural connectivity linking different regions of the cortex to each other and to deeper subcortical structures of the brain (74,75). Since these networks delineate the exact framework of the social brain in humans, I maintain that this maladaptive disorder can be rightly regarded as a costly by-product of social brain evolution in Homo sapiens. We are a species highly adapted and attuned to a complex social world. In schizophrenia, we encounter a disorder of this evolved social brain network. Thus, individuals with this disease find themselves seriously disadvantaged in the social arena, unable to correctly read and respond to social signals, and vulnerable to the stresses of their complex social environments. This state of "disembodiment" and interpersonal alienation is the core phenomenon of schizophrenia and the root cause of intolerable suffering in the lives of those affected.