Differential amygdala response during facial recognition in patients with schizophrenia: an fMRI study
Introduction
Patients with schizophrenia often perform poorly in social situations. Previous studies reported that they had been less accurate than normal controls in facial identity matching requiring whether pairs of faces were the same or different persons (Feinberg et al., 1986) and the patients with paranoia had experienced other people as directing attention toward them when in reality attention was not being directed at them Rosse et al., 1994, Franck et al., 1998. Moreover, they have performed worse than normal controls in recognition of facial expression of emotion Walker et al., 1984, Feinberg et al., 1986, Heinmberg et al., 1992; for example, in emotion matching to decide the same or different emotions in pairs of faces or emotion labeling to decide linguistic labels of emotional faces. These impairments in recognizing facial and/or emotional expression may be related to the misinterpretation of social interactions or to the flat effect commonly found in schizophrenia.
The patients with bilateral amygdalotomy or bilateral amygdala damage were poor in the recognition of facial identity or facial emotion, especially fearful face Adolphs et al., 1994, Adolphs et al., 1999, Anderson and Phelps, 1998. Recent neuroimaging studies using positron emission tomography (PET) or functional magnetic resonance imaging (fMRI) reported that the amygdala was activated during emotional face perception Schneider et al., 1995, Morris et al., 1998, Paradiso et al., 1999, Blair et al., 1999. It is strongly conceivable, therefore, that the amygdala is related to recognition of faces and emotions LeDoux, 2000, Davis and Whalen, 2001.
Amygdala abnormalities in schizophrenia have been reported in postmortem and neuroimaging studies Bogerts et al., 1985, Breier et al., 1992, Pearlson et al., 1997, in which schizophrenics showed reduced amygdala volume compared with controls.
To date, only two activation studies in emotional face recognition have been published in schizophrenia. An fMRI study reported that schizophrenic patients did not demonstrate amygdala activation during sad mood induction looking at sad facial expressions, despite significant amygdala activation in normal controls (Schneider et al., 1998). Another fMRI study also found that schizophrenics showed no amygdala activation during gender discrimination of faces depicting fearful faces, despite left amygdala activation in normal controls (Phillips et al., 1999). In the same study, non-paranoid schizophrenic patients categorized a disgusted face as an angry or fearful face in the identification task and it was demonstrated in the response to disgusted expressions activation in the amygdala, a region associated with perception of fearful faces.
The present study investigated the difference in amygdala response during facial recognition between patients with schizophrenia and normal controls using fMRI. The task used in the present study was a type of emotional intensity judgment task, while in the two previous activation studies of schizophrenia one used a mood induction task and the other an implicit task with regard to emotional face processing. In the emotional intensity judgment task, subjects were required to judge and interpret emotional faces, although the mood induction and gender discrimination task did not require such cognitive processes. Imaging data were analyzed in a voxel-by-voxel basis for single-group analysis and for between-group analysis according to the random effect model using Statistical Parameter Mapping (SPM) 99. Since the region focused in the present study was the bilateral amygdalae, the correction for the multiple comparisons was restricted to those structures.
We hypothesized that schizophrenic patients would show different amygdala activation compared with normal controls during recognition of faces with positive or negative emotion. The present findings showed that the patients demonstrated more prominent activation than the controls in the right amygdala during positive face discrimination.
Section snippets
Subjects
The patient group consisted of 12 patients with a DSM-IV (American Psychiatric Association, 1994) diagnosis of schizophrenia (six men and six women; aged 18 to 33 years, mean 26.0 years, SD=4.5; mean duration of illness 3.8 years, SD=3.5). They were outpatients or inpatients from the Department of Neuropsychiatry of Fukui Medical University. Ten patients were on neuroleptic medication (mean chlorpromazine equivalent daily dose 322.0 mg, SD=264.1) and two patients were unmedicated at the time of
Task performance
The mean (±SD) percentage of correct responses between the two groups showed no significant difference for the positive face discrimination (normal subjects, 97.2±4.8%; schizophrenic subjects, 95.1±5.3%) and for the negative face discrimination (92.0±7.8% and 95.8±5.3%, respectively). Two-way repeated-measure ANOVAs showed no significant main effect of group (F=0.29, df=1, 22, p=0.59) or condition (F=1.56, df=1, 22, p=0.23), or interaction (F=2.65, df=1, 22, p=0.12). Both groups performed at
Discussion
We hypothesized that schizophrenic patients would show different amygdala activations during facial recognition compared with normal controls. In fact, the present patient group showed greater amygdala activation than the control group.
Most of the present schizophrenic patients were taking neuroleptics at the fMRI examination. The effects of those medications on signal intensity changes are not yet understood, and some studies during motor task performance have suggested that neuroleptics
Acknowledgements
This study was supported by the Research Grant (JSPS-RFTF97L00203) for ‘Research for the Future‘ Program from the Japan Society for the Promotion of Science.
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