Visual processing and social cognition in schizophrenia: Relationships among eye movements, biological motion perception, and empathy
Introduction
In our daily life, adequate social interaction arises from action observation and reading others’ intentions and feelings. The human visual system can perceive motion of others’ actions, i.e., biological motion (BM) from only point-light displays, which depicts movements of actor's main joints. Point-light displays have been widely used to investigate bodily motion perception (Johansson, 1973, Verfaillie, 2000). Previous studies have shown that BM provides relevant social information regarding intention (Blakemore and Decety, 2001, Runeson and Frykholm, 1983) and emotion (Dittrich et al., 1996, Pollick et al., 2001) as well as perceptual characteristics.
In BM perception, similarly to face recognition, visual attention plays an important role. Attention is modulated by bottom-up and top-down processing (Desimone and Duncan, 1995, McMains and Kastner, 2011). Bottom-up attention is stimulus-driven mechanisms and contributes to the early stage of visual perception (Itti and Koch, 2001), whereas top-down attention is goal-directed mechanisms. Although automatic bottom-up processing has been empathized, top-down processing is also involved in BM perception when the task difficulty is high (Thompson and Parasuraman, 2012). Attention is closely related to eye movements for selecting visual information (Fischer and Weber, 1993, Kowler et al., 1995).
Schizophrenia patients have attentional impairment (Heinrichs and Zakzanis, 1998) and aberrant eye movement patterns (Levy et al., 2010). Previous studies on eye movements during face recognition have demonstrated that schizophrenia patients fixate less on feature regions including eyes and mouth compared to healthy controls (Green et al., 2003, Loughland et al., 2002, Phillips and David, 1998). These results indicate impaired bottom-up attention in schizophrenia. Moreover, a previous study reported that attention training in which schizophrenia patients were instructed to look at stimuli's eyes and mouth improved the performance of face recognition (Combs et al., 2008). This result would suggest that top-down attention compensates for abnormal bottom-up attention in schizophrenia.
Recently, it has become evident that schizophrenia patients have impaired BM perception (Kim et al., 2013, Kim et al., 2011, Kim et al., 2005). However, it remains unclear how abnormal attention or eye movements influence BM perception in schizophrenia. In the present study, we investigated the strategy of eye movements during BM perception in schizophrenia. Our prediction was that patients would exhibit different gaze patterns compared to healthy subjects, if top-down attention compensates for impaired bottom-up attention during BM perception in a similar manner as during face recognition.
Meanwhile, because BM perception is a hallmark of social cognition (Pavlova, 2012), altered BM perception could lead to social dysfunction in schizophrenia. Previous studies using point-light stimuli have shown that impairment in BM perception correlates with social functioning in schizophrenia (Kim et al., 2013, Kim et al., 2005). We previously reported that decreased activation in the extrastriate body area in response to body movements was associated with symptomatic severity in schizophrenia (Takahashi et al., 2010).
Although a direct link between higher social cognitive deficits and dysfunctional outcome is widely acknowledged (Couture et al., 2006), recent reports suggested a model in which the early stage of visual perception or attention could indirectly affect the final functional outcome, with social cognition as a mediator (Green et al., 2012, Sergi et al., 2006). Therefore, we hypothesized that aberrant eye movements would lead to deficits in BM perception and finally be linked to social cognitive impairments. Because empathy is a core feature of social cognition, and is conceptually divided into affective (bottom-up) empathy and cognitive (top-down) empathy (Decety and Lamm, 2006, Decety and Moriguchi, 2007), we focused on empathy. Specifically, we predicted that deficits in automatic bottom-up attention during BM perception would be observed in schizophrenia, and this would be associated with affective empathy rather than cognitive empathy.
Section snippets
Participants
Seventeen schizophrenia patients diagnosed with the patient edition of the Structured Clinical Interview for DSM-IV Axis I Disorders (SCID) were recruited. None of the patients had comorbid psychiatric disorders. Predicted IQ was measured by the Japanese Version of the National Adult Reading Test short form (Matsuoka and Kim, 2006, Matsuoka et al., 2006), which is considered to reflect the premorbid IQ of patients with schizophrenia. The Positive and Negative Syndrome Scale (PANSS) (Kay et al.,
Experiment 1: OM vs. BM perception task
As for accuracy, neither a main effect of group nor an interaction between group and stimulus was significant, indicating that schizophrenia patients could perceive OM and BM at the same level as healthy subjects. Details are given in Supplementary Material.
Test performance
Two-way ANOVA (group × difficulty level) for accuracy revealed a significant main effect of group [F(1, 33) = 9.94, p = 0.003], indicating lower accuracy for patients compared to controls. A main effect of difficulty was also revealed, indicating
Discussion
The present study examined the strategy of eye movements during BM perception in schizophrenia. Schizophrenia patients showed lower accuracy only in detecting BM stimuli, and had different gaze patterns compared to healthy controls. Schizophrenia patients fixated longer than healthy controls. In addition, patients who exhibited longer fixation durations and fewer numbers of fixations demonstrated higher accuracy. Furthermore, in the patient group, significant correlations were observed between
Conclusions
Although schizophrenia patients have deficits in BM perception, their altered gaze patterns indicate that top-down attention compensates for impaired bottom-up attention. Our findings suggested that aberrant eye movements lead to deficits in BM perception and finally link to social cognitive impairments. A recent study reported that BM perception is facilitated by attentional cueing (Parasuraman et al., 2009), suggesting that cognitive training that enhances top-down attention may improve
Acknowledgments
We would like to thank the participants and clinical research team of the Department of Psychiatry at Kyoto University for their support. We are especially grateful to Keita Ueda and Park Paeksoon for their valuable advice. This work was supported by grants-in-aid for scientific research A (24243061), B (23390290), S (22220003), and on Innovative Areas (23118004, 23120009), from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT); Grants-in-Aid for Young
References (46)
- et al.
Attentional-shaping as a means to improve emotion perception deficits in schizophrenia
Schizophr. Res.
(2008) - et al.
Visual scanpaths to threat-related faces in deluded schizophrenia
Psychiatry Res.
(2003) - et al.
Peripheral vision and oculomotor control during visual search
Vision Res.
(1999) - et al.
Impaired visual recognition of biological motion in schizophrenia
Schizophr. Res.
(2005) - et al.
The role of attention in the programming of saccades
Vision Res.
(1995) - et al.
Visual scanpaths to positive and negative facial emotions in an outpatient schizophrenia sample
Schizophr. Res.
(2002) - et al.
Individual differences in the perception of biological motion: links to social cognition and motor imagery
Cognition
(2013) - et al.
Abnormal visual scan paths: a psychophysiological marker of delusions in schizophrenia
Schizophr. Res.
(1998) - et al.
Perceiving affect from arm movement
Cognition
(2001) - et al.
Facial-affect recognition and visual scanning behaviour in the course of schizophrenia
Schizophr. Res.
(1997)
Attention, biological motion, and action recognition
Neuroimage
Perceiving human locomotion: priming effects in direction discrimination
Brain Cogn.
Emotion perception in schizophrenia: an eye movement study comparing the effectiveness of risperidone vs. haloperidol
Psychiatry Res.
From the perception of action to the understanding of intention
Nat. Rev. Neurosci.
The functional significance of social cognition in schizophrenia: a review
Schizophr. Bull.
Measuring individual differences in empathy: evidence for a multidimensional approach
J. Pers. Soc. Psychol.
Human empathy through the lens of social neuroscience
ScientificWorldJournal
The empathic brain and its dysfunction in psychiatric populations: implications for intervention across different clinical conditions
Biopsychosoc. Med.
Neural mechanisms of selective visual attention
Annu. Rev. Neurosci.
Perception of emotion from dynamic point-light displays represented in dance
Perception
Express saccades and visual attention
Behav. Brain Sci.
Attentional dynamics during free picture viewing: evidence from oculomotor behavior and electrocortical activity
Front. Syst. Neurosci.
From perception to functional outcome in schizophrenia: modeling the role of ability and motivation
Arch. Gen. Psychiatry
Cited by (33)
Association between global visual scanning and cognitive function in schizophrenia
2021, Asian Journal of PsychiatryThe attenuated visual scanpaths of patients with schizophrenia whilst recognizing emotional facial expressions are worsened in natural social scenes
2020, Schizophrenia ResearchCitation Excerpt :Consequently, scanpaths technology may be a useful tool for researching deficits in social cognition (Matsumoto et al., 2015). There have been several studies using visual scanpaths to explore social cognition (Matsumoto et al., 2015). Patients tend to exhibit fewer fixations, longer fixation duration, shorter scanpath lengths, longer saccade duration, and peak velocity, and smaller saccade amplitude compared with healthy controls (Beedie et al., 2012; Bestelmeyer et al., 2006; Nieman et al., 2007).
Oxytocin increases eye gaze in schizophrenia
2019, Schizophrenia ResearchCitation Excerpt :It will also be important to determine whether enhanced eye gaze is one of the mechanisms that drives oxytocin-induced improvements in social cognition in schizophrenia. Deficits in visual attention to social stimuli (Liu et al., 2016; Matsumoto et al., 2015) and the ability to detect eye contact (Tso et al., 2012) are associated with negative symptoms, and may impact functioning in schizophrenia via effects on social cognition (Green et al., 2012). For example, in people with schizophrenia, impaired performance on a mentalizing task that required reading cues from faces was entirely attributable to a lack of visual attention to the eyes (Roux et al., 2014).
Shared neural substrates of deficits in social cognition and negative symptoms in schizophrenia
2019, Social Cognition in PsychosisBiological motion processing in schizophrenia – Systematic review and meta-analysis
2017, Schizophrenia ResearchCitation Excerpt :Finally, complex social cognitive abilities, including mentalizing (Kim et al., 2013) and empathic accuracy (Olbert et al., 2013) may also be connected to biological motion processing in patients. A relationship between self-reported affective, but not cognitive, empathy and biological motion detection was also observed (Matsumoto et al., 2015). The event-related fMRI study which used BBM found a decreased BOLD-response modulation to biological vs. scrambled motion in patients compared to controls in the posterior superior temporal sulcus (Kim et al., 2011) and frontal regions (right ventral premotor cortex and left inferior frontal gyrus; Kim, 2014).
Empathy in schizophrenia: A meta-analysis of the Interpersonal Reactivity Index
2017, Psychiatry ResearchCitation Excerpt :This finding has been reported in several studies (e.g., see Andrews et al., 2013; Fujiwara et al., 2008; Gizewski et al., 2013; Montag et al., 2012a). Studies examining the fantasy component, on the other hand, are more disparate, with some finding significant deficits in schizophrenia samples (Derntl et al., 2012b; Fujiwara et al., 2008; Hooker et al., 2011; Lee et al., 2010) while others find fantasy to be intact or trending toward heightened fantasy in schizophrenia groups (Fischer-Shofty et al., 2013; Matsumoto et al., 2015; McCormick et al., 2012). The omission of the personal distress and fantasy components from meta-analyses of empathy in schizophrenia has left a gap in the literature, considering the likely importance of these factors in empathic tendencies for people with schizophrenia.