Review article
Social brain dysfunctions in schizophrenia: A review of neuroimaging studies

https://doi.org/10.1016/j.pscychresns.2006.05.001Get rights and content

Abstract

Several studies have indicated that schizophrenic patients show impaired performance in various aspects of social cognition, including theory of mind, emotion processing, and agency judgments. Neuroimaging studies that have compared patients and healthy subjects during such mental activity indicate an abnormal hemodynamic response in the medial prefrontal cortex, the prefrontal cortex, the amygdala, the inferior parietal lobe, i.e., a set of regions known to be critically involved in social cognition. This paper addresses a number of issues raised by schizophrenia research into theory of mind, emotion perception and self-agency with regards to the neural systems that mediate social cognition. In healthy subjects, typical brain patterns are associated with theory of mind, emotion perception and self-agency; some activated clusters overlap, while others are distinct. For instance, activations in the paracingulate gyrus are almost systematically associated with theory of mind tasks, while the amygdala is mainly involved in emotion perception tasks. Additional foci are frequently found activated during those tasks: superior temporal sulcus, inferior frontal area. Moreover, the inferior parietal lobe is thought to contribute to agency judgments. In the light of the data on brain abnormalities and neurochemical dysfunctions in schizophrenia, we discuss the interaction of social cognitive dysfunction with the supposed information processing abnormalities caused by dopamine dysregulation.

Introduction

Our knowledge concerning the cognitive and neural systems mediating social cognition has progressed considerably over the last 10 years. The concept of ‘social cognition’ refers to a relatively large number of psychological constructs ranging from the more complex–such as theory of mind or self-representation–to more elementary ones such as emotion perception, the processing of social cues and action-monitoring. Although the theoretical debate concerning the relations between these different abilities and the extent to which social cognition is domain-specific is unresolved, the validity of these constructs is supported by recent progress in various research fields including neuropsychology and functional cognitive neuroimaging. Furthermore, we believe that any new model will have to account for the fact that the human brain is strongly biased toward processing social stimuli including the behavior of conspecifics. Indeed, evolutionary psychology, developmental science, neuropsychology, neuroimaging, and psychopathology provide some empirical evidence to suggest that a somewhat restricted group of neural circuits is specialized to process social information.

Evolutionary psychologists have suggested that primates' unusually large brains are the product of the cognitive demands imposed by living in complexly bonded social groups (the social brain hypothesis). Importantly, (Dunbar 1998) demonstrated that there is a correlation between social complexity (e.g., group size) and relative brain size (i.e., the ratio of neocortex volume to the volume of the rest of the brain). The ability to understand, predict others' mental states and navigate within the social world has its roots in the long and progressive adaptation of the brain architecture imposed by evolutionary pressures. Many of the advanced cognitive skills enjoyed by humans are associated with improved executive functions associated with the expansion of the frontal cortex (Barrett et al., 2003). Notably, the anterior cingulate cortex, a key structure for cognitive and emotional control (Bush et al., 2000), is distinctive in that it contain neurons specific to pongids and hominids, the spindle cells (Nimchinsky et al., 1999). In an attempt to reconcile evolutionary considerations and neuro-architectonic findings, Allman et al. (2001) speculated that these spindle cells play a part in coordinating widely distributed neural activity involving emotion and cognition. Interestingly, some theorists proposed that psychosis may be considered as a price paid by humans for having developed such complex brain systems underlying complex social skills (Burns, 2004).

Over the last decade, great interest has been shown in the issue of the cerebral implementation of social cognition. Converging empirical evidence from electrophysiological and lesion studies in monkeys points to a restricted network of regions, namely the superior temporal cortex, the orbitofrontal cortex and the amygdala, that are reliably involved in social cognition (Brothers et al., 1990, Jellema et al., 2000). Similarly, neuropsychological observations in humans have emphasized the role of the orbitofrontal cortex in the regulation of social behavior (Eslinger and Damasio, 1985) and that of the amygdala in emotion perception (Adolphs et al., 1994). In addition, these findings have been extended by a large number of functional neuroimaging studies in healthy participants (see below).

Psychopathological research is another important source of knowledge concerning the mechanisms of social cognition. For instance, it has been suggested that some pathological conditions such as Asperger's syndrome and autism are the expression of an abnormal development of social cognitive skills in early infancy (Perner et al., 1989). Baron-Cohen and colleagues reported a dissociation between theory of mind skills and the understanding of physical causality in autistic children, whereas children suffering from Down's syndrome did not exhibit the same type of performance pattern (Baron-Cohen et al., 1986). It has been suggested that autism shares common features with schizophrenia such as impaired social performances or social withdrawal (Frith, 1992). In an early theoretical account, Frith also suggested that a specific impairment in metarepresentation is involved in the genesis of schizophrenic symptoms. More recently, Frith proposed that only explicit theory of mind (as opposed to the implicit processing of other people's mental states) is impaired (Frith, 2004b). Other scholars have attributed the disorganization syndrome to this deficit in attributing intentions to others and have discussed the relationship between this clinical dimension and the inability to process contextual information (Hardy-Baylé, 1994). It is worth noting that most of these accounts have focused on specific aspects of social cognition, i.e., theory of mind or emotion perception, while often excluding other aspects. The various theories therefore often fail to account for the widespread abnormalities found in the social cognition of schizophrenic patients at many different levels.

We believe that there are two ways in which psychopathology may benefit from neuroimaging investigations: Firstly, by demonstrating that schizophrenic patients present abnormal brain activity during various processing tasks involving social cognition. This consideration is crucial to studies that claim to have a basis in cognitive neuropsychology because the dysfunctions which occur at the neural level are used to validate the psychopathological construct. Secondly, the use of the knowledge acquired about normal brain functioning may help to formulate new questions about pathology and make it possible to generate testable hypotheses. This approach is similar to the one advocated by Willingham and Dunn (2003) which holds that one heuristic strategy in psychology requires researchers to “use existing knowledge of the brain to shape psychological theory.”

This article addresses the question of the social cognition impairments observed in schizophrenia by presenting a review of the experimental data obtained in the field of social cognitive neuroscience. Its primary motivation lies in the observation that social cognitive performances are related to the ability to solve concrete interpersonal problems (Corrigan and Toomey, 1995, Toomey et al., 1997), to the occurrence of socially deviant behavior (Brüne, 2005), and to the global social functioning of patients (Mueser et al., 1996, Penn et al., 1995). A better understanding of these issues should contribute to this research field by providing a more precise description of the psychopathological mechanisms involved in social cognition. We will focus on the involvement of three key regions–the medial prefrontal cortex, the amygdala, and the inferior parietal lobule–in the social cognitive deficits exhibited by schizophrenic patients. Although many experiments proved that several other regions were highly involved in social cognition (superior temporal sulcus, temporal poles, inferior parietal lobe, and cerebellum) the choice of those three cortical parts is grounded on their highly documented contributions to three main aspects of social deficits arising in schizophrenia: impairments of theory of mind, emotion perception and agency. We will indicate a possible link with the fields of neuropathology and neurochemical disorders within a simple, yet speculative, model.

Section snippets

Functional abnormalities in the medial prefrontal cortex and mentalization impairments in schizophrenia

The most frequently replicated finding from the neuroimaging studies of theory of mind is the involvement of the medial prefrontal cortex. Indeed, as Fig. 1 indicates, nearly all mentalizing tasks are associated with single or multiple clusters of activation in this region. In addition, half of the neuroimaging studies of emotion processing reviewed here also found activation in this region. Thus, mentalizing and the perception of emotion commonly seem to recruit similar portions of the medial

Functional abnormalities in the amygdala and social cognition deficits

No one doubts that the amygdala is involved in emotional experience and social perception. However, its exact role is still unclear, especially when epistemic mental states (without affective content) are considered. Indeed, the amygdala is a key component in emotional processing and it has been claimed that it processes the online perception of other people's basic emotions (Blair and Cipolotti, 2000, Adolphs, 2002), especially when these emotions are negative as in the case of fear, sadness,

From shared representation to the question of self–other distinction: implication of the inferior parietal lobe

Recent work on the neural networks underpinning social cognition has emphasized the role of brain circuits which are recruited both for the representation of the self and others. This mechanism accounts for the automatic mapping between self and other (Decety and Jackson, 2004). It is primarily based on perception–action coupling and has been described within the framework of the common coding theory (Prinz, 1997). This theory states that perception of an action should activate one's own action

Links between social cognition and neurobiological abnormalities in schizophrenia

There is evidence that schizophrenic patients exhibit variable social performances at different period of the illness (Edwards et al., 2002, Corcoran et al., 1995, Pickup and Frith, 2001) despite the fact that, globally, impairments in emotion perception and theory of mind are not correlated with medication (Kerr and Neale, 1993, Poole et al., 2000, Sarfati et al., 1997a, Sarfati et al., 1997b). To our knowledge, experimental attempts to test the hypothesis that theory of mind performance is a

Conclusion

Schizophrenia is a clinical qualification of the mental conditions associated with chronic impairments of volition, thought organization, emotional drive and representation of reality. Within a cognitive neuropsychological framework, which is supported by recent findings in the field of cognitive neuroscience, schizophrenia encompasses disruptions of the ability to represent one's own and other people's mental states including intentions and emotions, and to dissociate accurately between

Acknowledgments

We would like to thank Philip Jackson for helpful discussions. Eric Brunet-Gouet was supported by the Association Francaise de Psychiatrie Biologique associée aux Laboratoires Sanofi-Synthélabo, by the Fondation Lilly, and by the Université Versailles-Saint Quentin.

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