Elsevier

Psychiatry Research

Volume 190, Issue 1, 30 November 2011, Pages 23-31
Psychiatry Research

The study of social cognition with neuroimaging methods as a means to explore future directions of deficit evaluation in schizophrenia?

https://doi.org/10.1016/j.psychres.2010.11.029Get rights and content

Abstract

This article discusses the important advances in a recent field of science dealing with the brain processes implicated in understanding social situations and interacting with others. Many behavioral studies on schizophrenia have shown the impairment of these processes and their preferential relation with disorganization and negative syndromes. Brain imaging is a powerful method to identify brain systems participating in these processes in healthy subjects and will be used increasingly to study mental disorders such as schizophrenia. A few preliminary studies have opened this field of research and allowed for the drawing of some limited conclusions. We emphasize the importance of developing an integrated neurocognitive framework to account for the multifaceted nature of social cognition deficits in schizophrenia. Inspired by contemporary models of empathy and social cognition that identify different components such as shared representation, mentalizing, self/other distinction, we show how schizophrenia affects these components at the behavioral and functional levels. We also outline the interest of this model to understand putative abnormalities of contextual integration within the area of mentalization. Finally, we discuss how specialized measures of brain functions during the performance of these precisely defined mental processes might be used as outcome predictors.

Introduction

Schizophrenia is associated with a severe social handicap resulting in a drastic reduction of autonomy and of professional and personal achievements, and in the disruption of family and peer relations. Contrary to widespread intuition, several authors showed that these central aspects of prognosis are only weakly predicted by symptoms (Rosen and Garety, 2005, Wykes and Reeder, 2005, Brüne et al., 2007). The limited performance of clinical evaluations to discriminate the severity of the illness or to define therapeutic strategies has led to the proposal of new evaluation techniques and tools, many of them inspired by neuropsychological assessment. This was, for instance, the rationale for the initiative Measurement and Treatment Research to Improve Cognition in Schizophrenia (MATRICS) of the National Institute of Mental Health (NIMH) that offered, from a consensus of experts, a neuropsychological battery to promote cognitive disorders as a target of pharmaceutical treatment (Marder et al., 2004). In addition, this proposal recognized explicitly the role of social cognition, among other domains such as attention, executive function, and working memory, to determine a patient's status beyond clinical evaluations. Given their objectives oriented at pharmaceutical research, MATRICS experts did not provide an integrated view of social cognition based on recent research in this domain. In the present article, we will take into account the emergence of a new field of research dealing with the neurocognitive processes involved in social behavior that recently offered both theoretical and experimental insights into the abnormal processes of schizophrenia. Importantly, social cognition appears promising to offer a convergent point of scattered research in several domains such as theory of mind, emotion perception, metacognition, cognitive remediation, and functional outcome evaluation.

This article provides an overview of research in the field, taking selectively into account results from behavioral research (section 2) to neuroimaging studies (4 Representing social information, 5 Self/other distinction mechanisms, and 6). We stress the relevance of models, coming from social and affective neurosciences, and propose a cognitive framework inspired by current models (section 3). In 7 Is there a link between mentalization deficits and disorder of contextual integration in schizophrenia?, 8 Memory engagement in social cognition, and 9, we outline three perspectives of research that would merit investigations using functional neuroimaging. We conclude by emphasizing the importance of this literature in assessing the illness course and outcome (section 10).

Section snippets

Insights from behavioral and clinical studies

As will be discussed in the following, social cognition does not constitute a unitary construct (Farrow, 2007) and is not even a function per se. Often classified as a hybrid between an emotional and a cognitive phenomenon, social cognition encompasses many aspects as follows: gesture social perception, eye-gaze detection, emotion perception, empathy, agency and self/other distinction, mentalizing (also known as theory of mind), recognition of intentional causality or intentionality, etc. Most

The needs for an integrative model of social cognition

Several conceptual frameworks have been proposed to guide experimentations on social cognition in schizophrenia research. Some psychopathological models such as the one described by Couture et al. (2010) aimed to explain the disorder in order to predict functional outcome. According to these authors, interpretations of social or emotional cues depend on the patient's attributional style (for instance, a personalizing bias), which in turn is influenced by theory of mind inferences. Although this

Representing social information

At the input of the information processing chain, new events come from the environment (external events such as others' gestures, facial expressions, speech utterances) or from ourselves (internal cognitive events such as thoughts and emotions, as well as our own actions, reactions, sensations). These events activate corresponding representations, which in turn can activate associated representations stored in memory (information stored in episodic memory about the specific context or person,

Self/other distinction mechanisms

The theory of shared representation implies the existence of a system that keeps track of the recipient to which the current representation is attached. As stressed by Decety and Jackson (2004), in the absence of such a system linked to regulation mechanisms, the activation of shared representations by other's imagined or observed action or emotion could lead to contagion and the inability to separate our feelings from those of others. In other words, this necessary system allows self/other

Mental state attribution through mentalizing

The model proposed in this article recognizes the importance of a mentalizing mechanism that can be conceptualized as an executive component managing the multiple aspects of representations that are concurrently activated by the inherently complex everyday social interactions (or by the different pieces of information provided in a mentalizing task). These activated representations can be either social or contextual and can be activated through perception or verbal descriptions or retrieved

Is there a link between mentalization deficits and disorder of contextual integration in schizophrenia?

The model of social cognition presented in this article describes the role of mentalization in generating an integrated representation of social percepts by evaluating and selecting hypotheses on the hidden mental states that give coherence to the observed behavior. Such an approach to theory of mind emphasizes the integrative role of mentalizing a manner analogous to the way that Dennett (1987) has described the “intentional stance” as an efficient means to give sense to the social world. As

Memory engagement in social cognition

Although the relationship between social cognition and memory has not often been addressed directly, there is an obvious and fundamental relationship between the mentioned systems of representation and different types of memory. Considering the tight relations between self-reflection and thinking about others, it is tentative to hypothesize a crucial influence of autobiographical memories on the capacity to understand others by recalling our own experiences in similar contexts (Dimaggio et al.,

Social cognition is under the influence of structural characteristics

As reported above, investigation of social-cognitive processes in schizophrenia led to incongruent findings in several brain regions. Taking into account recent research that benefited from advances in structural characterization of human grey and white matter, such findings deserve further explorations with special attention given to the correlations of abnormalities of brain structures with local functional measures. Concerning the correlates of cortical structure, Benedetti et al. (2009)

Mental handicap assessment as a perspective for neurocognitive research

In this article, we tried to integrate a large set of theoretical proposals and empirical evidence into a neurocognitive model of abnormal social cognition in schizophrenia. This selective review reveals the extreme difficulty to provide a unique conceptual framework that could account for the heterogeneous clinical and performance patterns found in this disorder. However, advances in social neuroscience based on healthy subjects allow a coherent investigation of the disorders within the scope

Acknowledgements

We would like to thank Nadine Bazin, Emilie Baup-Bobin and Amélia Lemoalle for their important contribution to the ideas and the results presented here.

DV received a PhD student grant from Neuropôle. AMA is supported by a postdoctoral research grant from the Canadian Institutes for Health Research (CIHR). PLJ received a salary grant from the CIHR (New Investigator). EB received funding from INSERM's “Contrat d'Interface pour hospitaliers” program. The authors would also like to acknowledge the

References (117)

  • E. Bora et al.

    Empathic abilities in people with schizophrenia

    Psychiatry Research

    (2008)
  • E. Bora et al.

    Theory of mind impairment in schizophrenia: meta-analysis

    Schizophrenia Research

    (2009)
  • M.B. Brodeur et al.

    Memory for everyday actions in schizophrenia

    Schizophrenia Research

    (2009)
  • M. Brüne et al.

    Mental state attribution, neurocognitive functioning, and psychopathology: what predicts poor social competence in schizophrenia best?

    Schizophrenia Research

    (2007)
  • M. Brüne et al.

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

    Neuroscience and Biobehavioral Reviews

    (2006)
  • M. Brüne et al.

    An fMRI study of theory of mind in schizophrenic patients with “passivity” symptoms

    Neuropsychologia

    (2008)
  • M. Brüne et al.

    Social skills and behavioral problems in schizophrenia: the role of mental state attribution, neurocognition and clinical symptomatology

    Psychiatry Research

    (2011)
  • E. Brunet et al.

    Abnormalities of brain function during a nonverbal theory of mind task in schizophrenia

    Neuropsychologia

    (2003)
  • Y. Cheng et al.

    The perception of pain in others suppresses somatosensory oscillations: a magnetoencephalography study

    Neuroimage

    (2008)
  • H. Critchley et al.

    Fear conditioning in humans: the influence of awareness and autonomic arousal on functional neuroanatomy

    Neuron

    (2002)
  • B. Derntl et al.

    Generalized deficit in all core components of empathy in schizophrenia

    Schizophrenia Research

    (2009)
  • G. Dimaggio et al.

    Know yourself and you shall know the other... to a certain extent: multiple paths of influence of self-reflection on mindreading

    Consciousness and Cognition

    (2008)
  • G. Dimaggio et al.

    Impaired self-reflection in psychiatric disorders among adults: a proposal for the existence of a network of semi independent functions

    Consciousness and Cognition

    (2009)
  • S. Dollfus et al.

    Functional deficit in the medial prefrontal cortex during a language comprehension task in patients with schizophrenia

    Schizophrenia Research

    (2008)
  • P.G. Enticott et al.

    Reduced motor facilitation during action observation in schizophrenia: a mirror neuron deficit?

    Schizophrenia Research

    (2008)
  • C. Farrer et al.

    Neural correlates of action attribution in schizophrenia

    Psychiatry Research: Neuroimaging

    (2004)
  • FettA.K. et al.

    The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: a meta-analysis

    Neuroscience & Biobehavioral Reviews

    (2011)
  • H. Fujiwara et al.

    Anterior cingulate pathology and social cognition in schizophrenia: a study of gray matter, white matter and sulcal morphometry

    Neuroimage

    (2007)
  • H.L. Gallagher et al.

    Functional imaging of ‘theory of mind’

    Trends in Cognitive Sciences

    (2003)
  • K. Hirao et al.

    Theory of mind and frontal lobe pathology in schizophrenia: a voxel-based morphometry study

    Schizophrenia Research

    (2008)
  • M. Hoekert et al.

    Impaired recognition and expression of emotional prosody in schizophrenia: review and meta-analysis

    Schizophrenia Research

    (2007)
  • P.L. Jackson et al.

    Motor cognition: a new paradigm to study self–other interactions

    Current Opinion in Neurobiology

    (2004)
  • P.L. Jackson et al.

    How do we perceive the pain of others? A window into the neural processes involved in empathy

    Neuroimage

    (2005)
  • P.L. Jackson et al.

    To what extent do we share the pain of others? Insight from the neural bases of pain empathy

    Pain

    (2006)
  • S.E. Kim et al.

    The neural mechanism of imagining facial affective expression

    Brain Research

    (2007)
  • D. Koren et al.

    The neuropsychological basis of competence to consent in first-episode schizophrenia: a pilot metacognitive study

    Biological Psychiatry

    (2005)
  • D. Koren et al.

    The neuropsychological basis of insight in first-episode schizophrenia: a pilot metacognitive study

    Schizophrenia Research

    (2004)
  • M. Kutas et al.

    Electrophysiology reveals semantic memory use in language comprehension

    Trends in Cognitive Sciences

    (2000)
  • K.S. LaBar et al.

    Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study

    Neuron

    (1998)
  • LeeS.J. et al.

    Multi-level comparison of empathy in schizophrenia: an fMRI study of a cartoon task

    Psychiatry Research

    (2010)
  • K.R. Leslie et al.

    Functional imaging of face and hand imitation: towards a motor theory of empathy

    Neuroimage

    (2004)
  • A. Lindner et al.

    Disorders of agency in schizophrenia correlate with an inability to compensate for the sensory consequences of actions

    Current Biology

    (2005)
  • P.H. Lysaker et al.

    Poor insight in schizophrenia: links between different forms of metacognition with awareness of symptoms, treatment need, and consequences of illness

    Comprehensive Psychiatry

    (2011)
  • P.H. Lysaker et al.

    Metacognition and schizophrenia: the capacity for self-reflectivity as a predictor for prospective assessments of work performance over six months

    Schizophrenia Research

    (2010)
  • S. Mehl et al.

    Social performance is more closely associated with theory of mind and autobiographical memory than with psychopathological symptoms in clinically stable patients with schizophrenia-spectrum disorders

    Psychiatry Research

    (2010)
  • J. Miyata et al.

    Reduced white matter integrity as a neural correlate of social cognition deficits in schizophrenia

    Schizophrenia Research

    (2010)
  • C. Montag et al.

    Self-reported empathic abilities in schizophrenia

    Schizophrenia Research

    (2007)
  • K.N. Ochsner

    The social–emotional processing stream: five core constructs and their translational potential for schizophrenia and beyond

    Biological Psychiatry

    (2008)
  • P. Rainville

    Brain mechanisms of pain affect and pain modulation

    Current Opinion in Neurobiology

    (2002)
  • L.A. Ross et al.

    Social cognition and the anterior temporal lobes

    Neuroimage

    (2010)
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