Altered face inversion effect and association between face N170 reduction and social dysfunction in patients with schizophrenia
Highlights
► Normal controls showed a significant increase in N170 amplitude to inverted faces compared to upright faces while schizophrenic patients showed no such findings, whereas both groups showed no significant differences in N170 amplitude evoked by inverted and upright motor cars. ► There was a significant association between social dysfunction and face-N170 reduction in schizophrenia. ► This study revealed the association between deficits of face-specific configuration processing and social dysfunction in schizophrenia.
Introduction
Face recognition represents an evolutionarily significant element of nonverbal decoding that may be viewed as a neuropsychological building block for social interaction. Indeed, a critical component of effective nonverbal decoding may presuppose a capacity to extract social and affective cues from faces. There is accumulating evidence to suggest that schizophrenic patients may have deficits in both facial recognition and recognition of facial expressions (Gruzelier et al., 1999, Habel et al., 2000, Whittaker et al., 2001), which in turn have been related to disease-specific disturbances in sociality (Green et al., 2000). Face recognition may be qualitatively different from other recognition systems in terms of the underlying neurobiological structure and developmental trajectory.
Of note, facial recognition processing can be assessed by examining the visual-evoked event-related potential (ERP). Data from ERP studies have demonstrated that the negative potential recorded at occipitotemporal leads, the N170, is more negative (i.e., larger) for faces than for complex objects in healthy subjects (Bentin et al., 1996). However, several studies have found that schizophrenics show smaller differences in the N170 amplitudes between faces and complex objects than normal controls (Herrmann et al., 2004, Onitsuka et al., 2006).
Although both face and complex object perception utilize the ventral pathway, faces are perceived, at least in part, by a separate processing stream in the ventral pathway (Ungerleider and Haxby, 1994). Based on converging evidence from electroencephalography (Rossion et al., 2003), and magnetoencephalography (Watanabe et al., 2003), the fusiform gyrus (FG) has been considered to be one of the main neural sources of the N170 to faces. Using functional magnetic resonance imaging (fMRI), Kanwisher et al. (1997) reported that the middle portion of the FG responded selectively to faces, leading them to call it the fusiform face area (FFA). In addition, the lateral occipital area is associated with the generation of face-N170 (Allison et al., 1999, Rosburg et al., 2010, Schweinberger et al., 2002).
Neuroanatomical, functional, and pathological abnormalities of the FG have been reported in schizophrenia. For example, structural MRI studies have demonstrated reduced FG gray matter volume in chronic schizophrenia (e.g., Onitsuka et al., 2003). A recent fMRI study reported that schizophrenics exhibited lower blood oxygenation level-dependent activation in the right FFA during the memorization of faces (Walther et al., 2009). Neuropathologically, Di Rosa et al. (2009) found reduced neuronal density in the FG of patients with schizophrenia. Thus, dysfunction of the FG may be associated with the pathophysiology of schizophrenia, at least to some extent.
The social dysfunction of schizophrenia may be associated with deficits of face processing, since effective social communication depends largely upon the capacity to extract social and affective cues from faces, and represents a critical component of effective social communication. Our group reported correlations between reduced N170 amplitudes to faces and lower Global Assessment of Functioning (GAF) scores in patients with schizophrenia (Obayashi et al., 2009). However, as far as we know, there have been few studies that have investigated the association between social functioning and neurophysiological deficits of face processing in schizophrenic patients. Neurophysiologically, face-specific configuration processing can be evaluated by the face inversion effect (FIE) in the N170 amplitude, because it has been repeatedly reported that the face-N170 amplitude is specifically enhanced in healthy subjects viewing inverted faces (Linkenkaer-Hansen et al., 1998, Rossion et al., 1999). This effect is, in part, thought to be due to the fact that inverted faces are more difficult to process than upright faces, resulting in an attentional ‘processing negativity’ overlapping with the N170 component (George et al., 1996, Eimer, 2000). The inversion requires mental rotation of the facial stimuli, and the FIE is a special type of processing in the human brain (Rossion and Jacques, 2008). The present study examined the FIE and the relationships between the face-N170 and the scores on the Social Functioning Scale (SFS) (Birchwood et al., 1990) in schizophrenic patients.
The present study was designed to test the hypothesis that patients with schizophrenia will show less FIE in visual processing than healthy subjects, and that functional abnormalities will be associated with social dysfunction in patients with schizophrenia.
Section snippets
Subjects
Fifteen patients with schizophrenia and 15 normal control subjects with normal/corrected vision, age 25–35, all right-handed (Oldfield, 1971), participated in this study. After a complete description of the study, all participants signed an informed consent form in accordance with the regulations of the Ethics Commission of the Graduate School of Medical Sciences, Kyushu University. The demographic data for all subjects are presented in Table 1.
The exclusion criteria were as follows: (1)
Demographics and behavioral performance
There were no significant group differences in age, handedness score, SES, or parental SES (see Table 1). No significant correlations existed between the chlorpromazine-equivalent dosage and N170 amplitudes in response to any stimuli (−0.15⩽rho⩽0.43, 0.11⩽p⩽0.95). There were also no group differences in the accuracy of target responses (patients, 95.6%; controls, 95.5%; t[28] = 0.21, p = 0.91) or the mean reaction times (patients, 404 ms; controls, 404 ms; t[28] = −0.07, p = 0.99).
Patients showed
Discussion
The current study investigated the inversion effect of N170 visual evoked potentials elicited by faces and cars, scores on the Social Functioning Scale, and their interrelationship in patients with schizophrenia and normal controls. The major findings of this study were: (1) a reduced FIE of the N170 amplitude was observed in the patient group in contrast to normal controls; (2) in both groups, no inversion effect was observed for car stimuli; (3) schizophrenic patients showed trend-level
Acknowledgments
The authors gratefully acknowledge the administrative support of Kyoko Nakamura.
This work was supported in part by a grant from Research Group For Schizophrenia, Japan (to Dr. Onitsuka), Grants-in-aid for Scientific Research (B22390226 to Dr. Kanba and C23591712 to Dr. Onitsuka) from the Ministry of Education, Culture, Sports, Science and Technology, Japan, and Research Grants (H23 kokoro-ippan-002 to Dr. Kanba) from the Ministry of Health, Labor and Welfare, Japan.
The Ministry of Education,
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