Elsevier

NeuroImage

Volume 22, Issue 3, July 2004, Pages 1247-1254
NeuroImage

An fMRI study of differential neural response to affective pictures in schizophrenia

https://doi.org/10.1016/j.neuroimage.2004.03.028Get rights and content

Abstract

Although emotional dysfunction is considered a fundamental symptom of schizophrenia, studies investigating the neural basis of emotional dysfunction in schizophrenia are few. Using functional magnetic resonance imaging (fMRI) and a task viewing affective pictures, we aimed to examine automatic emotional response and to elucidate the neural basis of impaired emotional processing in schizophrenia. Fifteen healthy volunteers and 15 schizophrenics were studied. During the scans, the subjects were instructed to indicate how each of the presented pictures made them feel. Whole brain activities in response to the affective pictures were measured by fMRI. Controls recruited the neural circuit including amygdaloid–hippocampal region, prefrontal cortex, thalamus, basal ganglia, cerebellum, midbrain, and visual cortex while viewing unpleasant pictures. Despite an equal behavioral result to controls, the patients showed less activation in the components of the circuit (right amygdala, bilateral hippocampal region, medial prefrontal cortex (MPFC), basal ganglia, thalamus, cerebellum, midbrain, and visual cortex). This study demonstrated functional abnormalities in the neural circuit of emotional processing in schizophrenia. In particular, decreased activation in the right amygdala and MPFC appears to be an important finding related to dysfunctional emotional behavior in schizophrenia.

Introduction

Emotional dysfunction such as “flattening affect” or “anhedonia” is considered to be one of the key symptoms of schizophrenia (Andreasen and Flaum, 1991). Recent functional imaging techniques have revealed dysfunction of the neural circuit (interrelationship among cortical region, thalamus, basal ganglia, and cerebellum) in schizophrenia Andreasen et al., 1999, Schultz and Andreasen, 1999. Most studies focused on cognitive dysfunction (Andreasen et al., 1999), while studies investigating the neural basis of dysfunctional emotional processing in schizophrenia are limited Gur et al., 2002, Paradiso et al., 2003, Phillips et al., 1999, Schneider et al., 1998, Taylor et al., 2002. Previous neuroimaging studies in normal subjects revealed the neuroanatomical correlates of emotional processing and the crucial role of the amygdala in processing negative emotions. In particular, left-sided activations in the amygdala while processing negative facial expressions have been consistently reported (Calder et al., 2001). Recent functional magnetic resonance imaging (fMRI) studies revealed that schizophrenic patients demonstrated decreased activation in the bilateral amygdala during an emotion induction task by facial expressions (Schneider et al., 1998) or decreased activation in the left amygdala during a discrimination task of emotional facial expressions (Gur et al., 2002). However, discriminating analogous facial expressions is an effortful cognitive process whether subjects categorize the facial expressions by gender or emotion. Cognitive demands for elaborate recognition or detailed rating may modulate the emotional response in the brain Critchley et al., 2000, Hariri et al., 2000, Keightley et al., 2003, Lange et al., 2003, Taylor et al., 2003. In addition, it should be noted that emotional facial expressions do not necessarily elicit the subjective experience of emotions (Davidson and Irwin, 1999).

Several activation studies used affective pictures to elicit emotion in healthy volunteers Lane et al., 1997a, Lane et al., 1997b. The task of simply viewing emotionally salient pictures could minimize cognitive demands and would be suitable for examining automatic emotional response. Only a few positron emission tomography (PET) studies have investigated the emotional processing of affective pictures with a task of rating subjective emotional experience (Taylor et al., 2002) or with a task of emotional perception (Paradiso et al., 2003) in schizophrenia, and these studies have not established consistent results for a better understanding of dysfunctional emotional processing in schizophrenia. To our knowledge, no fMRI study has examined the neural response across the whole brain to affective pictures in schizophrenia. In the present study, we used fMRI and a task with minimal cognitive demands to identify the neural circuit of automatic emotional processing. We expected the subjects to react to affective pictures without an effortful cognitive process and categorize them roughly according to their subjective emotional experiences. Comparing the neural responses of schizophrenic patients with those of healthy controls, we aimed to elucidate the neural basis of impaired emotional processing in schizophrenia.

Section snippets

Subjects

Fifteen schizophrenic patients (10 men and 5 women, mean age 29.0 years, SD = 6.9) meeting the DSM-IV criteria for schizophrenia were studied. Diagnoses were made by HT, YO, and the psychiatrists in charge based on a review of their charts and a conventionally semi-structured interview. Exclusion criteria were current or past substance abuse and a history of alcohol-related problems, mood disorder, or organic brain disease. Thirteen patients were recruited from the outpatient unit of Asai

Self-rating

The mean percentages of expected categorizations of the controls for the neutral, unpleasant, and pleasant pictures were 85.3% (SD = 8.3), 88.8% (SD = 11.3), and 59.0% (SD = 22.8), respectively, and those of the schizophrenic patients were 81.3% (SD = 8.3), 92.0% (SD = 9.5), and 55.0% (SD = 34.8), respectively. Two-way repeated-measures analysis of variance of the percentages of expected categorizations showed a significant main effect of condition (F = 27.6, df = 2, 84, P < 0.001), but not a

Discussion

In control subjects, we identified the neural circuit of the automatic emotional response to unpleasant pictures in the amygdaloid–hippocampal region, thalamus, OFC, MPFC, basal ganglia, cerebellum, midbrain, and visual cortex. We used evocative pictures with minimal cognitive demands so as to examine the automatic emotional response that requires no elaborate rating or categorization of stimuli for the subjects. Facial expressions do not necessarily elicit strong emotions, and cognitive

Acknowledgements

We thank Professor Toru Nishikawa of the Section of Psychiatry and Behavioral Science, Graduate School of Tokyo Medical and Dental University. The staffs of the Section of Biofunctional Informatics, Graduate School of Tokyo Medical and Dental University, and of Asai Hospital, are gratefully acknowledged. This work was supported by a Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science and Technology (15390348), a research grant for nervous and

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