Precentral and inferior prefrontal hypoactivation during facial emotion recognition in patients with schizophrenia: A functional near-infrared spectroscopy study
Introduction
Patients with schizophrenia demonstrate abnormal social cognition including face perception (Mandal et al., 1998, Walker et al., 1984), emotional face recognition (Kohler et al., 2010), and theory of mind (Bora and Pantelis, 2013, Pinkham, 2014). Behavioral and neuroimaging study results suggest that patients with schizophrenia have impairments in the neural network involved in face perception and emotional face recognition (Habel et al., 2010, Li et al., 2012, Mehta et al., 2014, Taylor et al., 2012). However, the neural substrates underlying face recognition in patients with schizophrenia have not been fully elucidated. We previously used functional near-infrared spectroscopy (fNIRS) to demonstrate abnormal fronto-temporal function in schizophrenia, using emotional-cognitive tasks (Egashira et al., 2015). As that study used an emotional go/no-go task, which involved emotional processing and cognitive inhibition, we did not quantify extent to which the emotional processing affected the results. To address this shortcoming, the current study used fNIRS to examine brain activity in patients with schizophrenia in response to facial emotional expressions.
The aim of this study was to identify which brain regions involved in emotional face recognition are impaired in patients with schizophrenia. In combination with the results of our previous study (Egashira et al., 2015), we aimed to determine which neural substrates are implicated in responses to emotional facial expressions and facial expressions with cognitive inhibition. We hypothesized that patients with schizophrenia would show poor behavioral performance and reduced activation of inferior frontal and ventral premotor areas during an emotional face expression task, consistent with involvement of the mirror neuron system (Mehta et al., 2014) and the emotional face processing network (Haxby et al., 2002).
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Participants
Nineteen patients with schizophrenia and 19 healthy participants statistically matched on age, sex, and premorbid IQ were studied. All participants were right-handed (Oldfield, 1971). Patients were recruited from Yamguchi University Hospital and Katakura Hospital. All met the schizophrenia criteria in the Diagnostic and Statistical Manual of Mental Disorders IV, Text Revision (DSM-IV-TR; American Psychiatric Association, 2000) as assessed by senior psychiatrists. Diagnoses were confirmed via
Behavioral performance
There were significant interactions between condition and diagnosis (F = 14.23, p < 0.001), task and diagnosis (F = 14.20, p < 0.001), and between condition, task, and diagnosis (F = 14.40, p < 0.001) (Table 2). There was a significant main effect of condition (F = 6.91, p = 0.013) and diagnosis (F = 14.20, p = 0.001), but not task (F = 0.21, p = 0.65). Given the significant three-way interaction, we carried out subsequent separate analyses for accuracy and MRT. For accuracy, there was a significant interaction
Discussion
Our primary finding was that patients with schizophrenia showed diminished activation of the right precentral and inferior frontal area in response to emotional face stimuli compared to healthy participants. These findings were not associated with clinical variables. We also found that patients with schizophrenia were slower than controls in face matching and emotional face identification, and were less accurate in the emotional face task. Performance was associated with severity of the
Conflict of interest
All authors declare that they do not have any commercial or financial involvements that might present an appearance of a conflict of interest in connection with the submitted article.
Contributors
Toshio Watanuki wrote the first draft of the manuscript, collected the data and analyzed the image data. Koji Matsuo designed the study, wrote protocol and supervised the content of the manuscript. Mani Nakashima undertook the image and ran statistical analyses. Terukazu Egashira, Kenichiro Harada, Masayuki Nakano and Toshio Matsubara managed the literature searches and collect the data. Kanji Takahashi and Yoshifumi Watanabe managed the study and review the draft. All authors contributed to
Role of funding source
This study was supported by JSPS KAKENHI grant numbers 24591716 and 15K09832 [KM], 25861011 [TM], and 25861012 [TW].
Acknowledgments
We would like to thank Mr. Masahiro Koike (Department of Radiological Technology, Yamaguchi University Hospital) for programming the NIRS task.
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