Abnormal facial emotion recognition is considered as one of the key symptoms of schizophrenia. Only few studies have considered deficits in the spatial frequency (SF)-dependent visual pathway leading to abnormal facial emotion recognition in schizophrenia. Twenty-one patients with schizophrenia and 19 matched healthy controls (HC) were recruited for this study. Event-related potentials (ERP) were measured during presentation of SF-modulated face stimuli and their source imaging was analyzed. The patients showed reduced P100 amplitude for low-spatial frequency (LSF) pictures of fearful faces compared with the HC group. The P100 amplitude for high-spatial frequency (HSF) pictures of neutral faces was increased in the schizophrenia group, but not in the HC group. The neural source activities of the LSF fearful faces and HSF neutral faces led to hypo- and hyperactivation of the frontal lobe of subjects from the schizophrenia group and HC group, respectively. In addition, patients with schizophrenia showed enhanced N170 activation in the right hemisphere in the LSF condition, while the HC group did not. Our results suggest that deficits in the LSF-dependent visual pathway, which involves magnocellular neurons, impair early visual processing leading to dysfunctional facial emotion recognition in schizophrenia. Moreover, it suggests impaired bottom-up processing rather than top-down dysfunction for facial emotion recognition in these patients.
Abnormal facial affect perception and processing have been widely documented in patients with schizophrenia, both behaviorally and physiologically, as measured by event-related potentials (ERPs). Over the last few decades, studies have revealed that face-related ERPs generally show reduced or delayed activation in patients with schizophrenia during facial emotion recognition or tasks related to face perception (McCleery et al., 2014). P100, a component reflecting early visual perception, was reduced in response to facial stimuli in patients (Campanella et al., 2006 and Caharel et al., 2007), while some studies reported no differences between normal controls (Herrmann et al., 2004, Wynn et al., 2008 and Jung et al., 2012). The N170 component has been consistently reported to show reduced amplitude and delayed latency that reflects altered decoding stages of facial features (Herrmann et al., 2004, Johnston et al., 2005, Turetsky et al., 2007 and Lee et al., 2010). Some studies report that the late ERP components of facial emotional processing (N250 or P300) are altered in schizophrenia (Streit et al., 2001, Turetsky et al., 2007 and Wynn et al., 2008); however, there are also results suggesting intact amplitudes and latencies in such components (Herrmann et al., 2004, Johnston et al., 2005 and Turetsky et al., 2007).
Facial affect recognition involves complex visual processing that combines the global emotional expression of the face with detailed features. Such visual features are transferred from the retina to the visual cortex through two major parallel pathways: the magnocellular pathway and parvocellular pathway (Livingstone and Hubel, 1988 and Tobimatsu and Celesia, 2006). Each pathway processes different aspects of facial features; global information and coarse emotional cues are related to the low-spatial frequency (LSF) features and thus, more dominantly processed through the magnocellular pathway, whereas high-spatial frequency (HSF) features like precise recognition of identity and detailed analysis of facial traits is more dominantly processed by the parvocellular pathway (Obayashi et al., 2009, Silverstein et al., 2010, Calderone et al., 2013 and Laprevote et al., 2013).
Researchers have found meaningful abnormalities of such visual pathways in schizophrenia patients. These deficits include increased visual thresholds (Schechter et al., 2003 and Caharel et al., 2007), greater sensitivity to backward masking (Saccuzzo and Braff, 1986, Braff, 1993, Butler et al., 1996, Green and Nuechterlein, 1999 and Schechter et al., 2003), decreased contrast sensitivity (Slaghuis and Curran, 1999, Keri et al., 2002 and Butler et al., 2005), or motion perception (Chen et al., 1999, Schwartz et al., 1999 and Li, 2002). Such findings indicate impairments in both magnocellular and parvocellular pathway, but a more dominant impairment in the magnocellular pathway seems to be evident. Thus, the deficit in perceptual organization or ability to process global form information may be responsible for inaccurate facial expression recognition in schizophrenia (Frith et al., 1983, Turetsky et al., 2007, Laprevote et al., 2010 and Silverstein et al., 2010). However, there is insufficient evidence to confirm this hypothesis.
Since the parvocellular and magnocellular pathways have different dominancy in processing spatial frequencies (SF), it is possible to arouse each visual pathway using SF-manipulated facial images according to their dominancy. To the best of our knowledge, only one ERP study has used SF-manipulated facial images to investigate which visual pathway is responsible for abnormal emotion recognition in schizophrenia (Obayashi et al. (2009). Although they found that schizophrenia patients have deficits in SF-dependent visual processing, they failed to demonstrate any change in emotional processing due to SF differences. Therefore, the relationship between visual pathway deficits and altered facial affect recognition by patients with schizophrenia is still unclear.
In the current study, we investigated how deficits in the visual pathway alter face affect processing in schizophrenia using SF-manipulated facial images as stimuli. Patients with schizophrenia show more inaccurate understanding in negative emotions (Bell et al., 1997); therefore, we used fear and neutral facial pictures in different SF conditions. We hypothesized that visual pathway deficiencies would be dominant for LSF fearful face pictures expressed as reduced amplitude of the ERP components or reduced source activation of pathway-related brain areas.
