Review
Theory of mind—evolution, ontogeny, brain mechanisms and psychopathology

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Abstract

The ability to infer other persons' mental states and emotions has been termed ‘theory of mind’. It represents an evolved psychological capacity most highly developed in humans. The evolutionary origins of theory of mind can be traced back in extant non-human primates; theory of mind probably emerged as an adaptive response to increasingly complex primate social interaction. This sophisticated ‘metacognitive’ ability comes, however, at an evolutionary cost, reflected in a broad spectrum of psychopathological conditions. Extensive research into autistic spectrum disorders has revealed that theory of mind may be selectively impaired, leaving other cognitive faculties intact. Recent studies have shown that observed deficits in theory of mind task performance are part of a broad range of symptoms in schizophrenia, bipolar affective disorder, some forms of dementia, ‘psychopathy’ and in other psychiatric disorders. This article reviews the evolutionary psychology of theory of mind including its ontogeny and representation in the central nervous system, and studies of theory of mind in psychopathological conditions.

Introduction

The term ‘theory of mind’ was originally proposed by primatologists Premack and Woodruff in a seminal article to suggest that chimpanzees may be capable of inferring mental states of their con-specifics (individuals of the same species) (Premack and Woodruff, 1978). Later on, the term was adopted by child psychologists to describe the ontogenetic development of mental perspective taking in infants and young children (e.g. Leslie, 1987). In terms of psychopathology, the concept of a disturbed theory of mind has become increasingly influential to explain behavioral symptoms in children with autistic spectrum disorders (Baron-Cohen et al., 1985). It is now widely acknowledged and well buttressed by numerous empirical studies that autistic children and adults with Asperger's syndrome, a mild form of autism, have profound difficulties in appreciating the mental states of other individuals (e.g. Baron-Cohen, 1988, 1991; Baron-Cohen et al., 1997, 2001a; Buitelaar et al., 1999). Such deficits in mental state comprehension have been shown to be selective, that is, other cognitive capacities or ‘non-social’ intelligence may well be preserved in people with autism (Baron-Cohen et al., 1986; Baron-Cohen, 1991). The situation with other psychopathological conditions and psychiatric disorders is less clear. There is, however, growing evidence that impaired theory of mind may also lie at the core of certain psychotic symptoms in ‘endogenous’ psychoses and behavioral deviations found in heterogeneous disorders affecting frontal lobe functioning—from psychopathy to frontotemporal dementia.

Although somewhat speculative, it is conceivable that the strong desire inherent to human nature to attribute agency—we sometimes even ascribe intentions to inanimate objects—renders the cognitive faculty of theory of mind vulnerable to dysfunction. In other words, if theory of mind, as suggested here, is so central to human life, any functional impairment or structural disruption of the underlying neural substrates of this recently evolved cognitive capacity could be detrimental to social functioning.

In this article, we seek to review the evolutionary background, the ontogenetic development and the evidence for selective disorders of theory of mind in psychopathological conditions. Before doing so, we want to emphasize that theory of mind only represents one particular aspect of what has been labeled ‘social cognition’ (Brothers, 1990; Adolphs, 2001). The perception of social signals, motivation, emotion, attention, memory and decision-making equally contribute to the actual behavioral output in social interaction. As Adolphs (2001) has pointed out, the components and boundaries of social cognition are to a great deal ill defined. For the sake of clarity and space, we consider it necessary to narrow the view on theory of mind—acknowledging that in ‘real-life’ situations theory of mind is entrenched in a neural network that constitutes the ‘social brain’ of human and non-human primates (Dunbar, 2003).

Section snippets

Theory of mind—adaptation to social complexity?

In 1966 and 1976, respectively, Jolly and Humphrey argued independently of each other that primates have excess cognitive capacities beyond the needs for everyday feeding and ranging. They suggested that it has been the social environment that primarily put evolutionary pressure on brain development in primates (Jolly, 1966; Humphrey, 1976). Indeed, primates are essentially gregarious animals, and group living certainly confers adaptive advantages on the individual such as better protection

Ontogeny of theory of mind

At birth, human infants are essentially immature. The growth of the human brain extends well into the postnatal period. At the cellular level, synaptic pruning and myelination even takes place until after puberty and adolescence (De Bellis et al., 2001; Levitt, 2003).

In principle, the ontogeny of the theory of mind faculty does not so much differ from the maturation of other brain functions—just as an infant is not capable of jumping before sitting, standing and walking, the ability of

CNS-representation of theory of mind

If primate brains, particularly neocortical structures, enlarged over evolutionary time due to selection pressures from the social environment, where exactly is theory of mind located in the human brain? Evidence comes from various sources. Comparative neuroanatomy and neurophysiology informs us which brain areas and corresponding functions came under selection pressure in non-human primates to evolve into the neural correlates of theory of mind in modern humans. In addition, functional brain

Testing theory of mind

The ‘gold standard test’ of comprehending other persons' minds is to grasp that others can hold false beliefs that are different from one's own (correct) knowledge (Dennett, 1978). The classic ‘Sally-and-Anne-Test’ (Wimmer and Perner, 1983) experimentally creates a situation in which a test person has to distinguish his or her own knowledge that an object has been hidden by one character (Anne) in the absence of another person (Sally) from the knowledge of the other characters involved. The

Psychopathology of theory of mind

The concept of theory of mind is appealing to clinical psychopathologists, because theory of mind in its most sophisticated expression is unique to humans and because its absence or impaired functioning may account for quite a broad spectrum of behavioral abnormalities in both children and adults. In the following section, we therefore briefly summarize some of the empirical findings regarding theory of mind in psychopathological conditions.

Developmental disorders

In this paragraph, we put emphasis on those studies addressing the issue of impaired theory of mind acquisition during child development. The starting point of empirical research into this matter was Baron-Cohen (1988) intriguing question whether the autistic child has a ‘theory of mind’. Since, Kanner's (1943) and Asperger's (1944) groundbreaking publications clinicians have sought to explain why autistic children would behave so socially withdrawn and unempathically the way they actually do.

Personality disorders and other non-psychotic disorders

Empirical research on theory of mind in personality disorders has largely focused on what has been conceptualized as ‘psychopathy’. Psychopaths have been characterized as superficially charming, but otherwise unreliable, ‘cold-hearted’ and unresponsive individuals. These emotional deficits have been found to be present in psychopaths from childhood on. It has therefore been argued that psychopathic individuals who are impaired in empathizing with others could have impaired theory of mind

Schizophrenia and affective disorders

Schizophrenia and affective disorders, commonly subsumed under the obsolete term ‘functional psychoses’ usually manifest in adolescence or adulthood. In contrast to theory of mind, deficits that emerge due to gross brain pathology (see below) or primarily due to developmental or personality disorders, schizophrenia and affective disorders have an intermediate position—we simply do not know whether theory of mind has developed normally in individuals suffering from ‘functional psychoses’.

Frith

Brain damage and degenerative brain disorders

Assessing theory of mind in patients suffering from brain lesions following stroke, brain tumor operation or degenerative disorders differs from the studies outlined above, because it can be taken for granted that theory of mind developed normally in these individuals.

A number of studies on theory of mind in patients with brain damage to the frontal lobes following cerebral artery infarction or following tumor excision have demonstrated that patients with right frontal lesions are impaired in a

Discussion

In this article, we have sought to examine a specific aspect of social cognition in an evolutionary perspective. The ability to infer mental states of other individuals, referred to as ‘theory of mind’ probably emerged in primates due to selection pressures from the social environment (Brothers, 1990). Tracing back the evolutionary history of this cognitive faculty, we found evidence that theory of mind most likely evolved from the capacity to monitor biological motion and from imitation

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