Schizophrenia (SZ) is one of the mental illnesses characterized by positive symptoms (such as delusions and hallucinations), negative symptoms (such as impaired motivation and social withdrawal), and various cognitive impairments (Owen et al., 2016). A lifetime morbid risk of SZ is approximately 0.7%. Patients with SZ need long-term treatment and care for residual symptoms and cognitive impairments. The clinical stage of SZ is divided into the following: prodrome, first episode, and chronic phase (Wojciak et al., 2016). Regarding cognitive function, patients with SZ have impairments in language, executive function, and attention domains. These cognitive impairments affect their daily functioning, including reasoning or problem-solving skills and socializing, and have been extensively examined in patients with SZ. Some studies have reported that impairment of visual processing in SZ is related to social perception (Corrigan et al., 1994; Sergi and Green, 2003) or social functioning (Sergi et al., 2006; Rassovsky et al., 2011). Visual processing is recognized as one of the major impairments in SZ (Butler et al., 2008; Silverstein and Keane, 2011b); various aspects of visual disturbance, such as deficits of motion perception (Chen, 2011) and perceptual organization (Uhlhaas and Silverstein, 2005; Silverstein and Keane, 2011a), have also been reported.

However, there has been limited investigation of color perception in SZ (Kogata and Iidaka, 2018). Shuwairi et al. (2002) reported that patients with SZ showed impaired color perception in standardized color discrimination tests. Specifically, patients with SZ made several mistakes in distinguishing between red, green, and blue colors; these mistakes differed from those made by patients with dopaminergic dysregulation, such as Parkinson’s disease and cocaine withdrawal (Price et al., 1992; Desai et al., 1997). Conversely, by focusing on the color priming effect, a study by Jahshan et al. (2012) reported that patients with SZ showed a different priming effect compared to healthy controls (HCs). They also suggested that the feed-forward connections of visual relay from the retina to the lateral geniculate nucleus in the thalamus and eventually to the primary visual cortex seem to be intact in patients with SZ. Thus, patients with SZ might have an impairment in color perception due to the disruption of pathways involving secondary or higher visual areas, besides those affecting the primary visual areas.

Furthermore, in a landmark study, David investigated unilateral (i.e., within the left or right visual field) or bilateral (i.e., both left and right visual fields) color recognition in patients with SZ using a tachistoscope (David, 1987). In the color naming task, the author found that patients showed impairment in naming colors upon instant presentation in the left visual field (LVF) condition but not in the right visual field (RVF); this finding suggested that the laterality effect resulted from dysfunction of the interhemispheric connectivity associated with abnormalities in the corpus callosum. In addition, Phillips et al. (1996) investigated the color-Stroop effect using the color-word paring paradigm and revealed that patients with SZ showed stronger color-Stroop facilitation when the stimuli were presented in the LVF than when they were presented in the RVF. Collectively, these findings indicate a lateralized color cognition with respect to cerebral dominance in patients with SZ. However, it remains unclear how the semantic properties of color, such as color name, could affect the performance of color perception.

Regarding the hemispheric laterality, prior studies investigated various lateralities in patients with psychiatric or developmental disorder. Indeed, Berretz et al. (2020) demonstrated atypical hemispheric asymmetries in these patients compared to HCs. Moreover, Berretz et al. (2020) pointed out that these asymmetries were affected by genetic and non-genetic factors. Sommer et al. (2001a) also reported different lateralities between patients with SZ and HCs; the prevalence of handedness, dichotic listening, and anatomical asymmetry. In particular, reduced hemispheric language laterality was identified as a key feature in patients with SZ. Furthermore, Oertel et al. (2010) investigated the laterality in patient with schizophrenia by auditory task and showed that symptom severity was related to a reduced laterality. Thus, atypical hemispheric laterality is an important parameter in patients with SZ.

In the present study, considering the effect of laterality on color recognition, we investigated the performance of patients with SZ and HCs in the color search task using a task developed by Gilbert et al. (2006). This search task manipulated two factors: the target position where the target color square emerges in either the LVF or RVF, and the color category, wherein the target and distractors may have the same or different color names. Since the primary visual cortex in both the hemispheres receives visual information from the contralateral visual field, the left hemisphere should have an advantage in accessing the information appearing in the RVF. In Gilbert et al. (2006)’s study, HCs responded faster in detecting the target in the RVF (i.e., left hemisphere) than in the LVF (i.e., right hemisphere) when the target and distractors had different color names. This laterality effect indicates a significant interaction between hemispheric laterality and lexical processing, which appears to occur in the language-dominant (i.e., left) hemisphere in healthy subjects. Therefore, using this task, we aimed to investigate the effect of laterality and also address the question of how the color lexicon of the target and distractors affect the performance of patients with SZ in the color search task.

In this experiment, we tested two hypotheses. First, patients with SZ would show a slower response when the target was shown in the RVF than when it was shown in the LVF, as reported previously (Posner et al., 1988). Second, the lexical difference in trial condition would affect the search performance depending on the target position. Several studies, using electroencephalogram (Spironelli et al., 2008) and functional magnetic resonance imaging (Sommer et al., 2001b), have demonstrated that language processing was less lateralized in patients with SZ than in HCs, and that the search performance for lexical difference could differ between patients with SZ and HCs. When the target and distractors differ with respect to their color names, patients with SZ would show an advantage (i.e., faster reaction time) when the target is presented in the LVF.

In this study, we examined the visual search performance for color perception in patients with chronic SZ and HCs. This study aimed to investigate how the position of the target and the color category of the target and distractors affected visual search performance. Differences in visual search performance were previously identified in normal adults (Gilbert et al., 2006), children (Franklin et al., 2008), and patients with aphasia (Paluy et al., 2011). In subjective reports and semi-structured interviews, patients with SZ reported distorted color perception (Chapman, 1966; Cutting and Dunne, 1986; Vollmer-Larsen et al., 2007). However, there is little evidence of impairment of color discrimination performance in patients with SZ, except in color perception (Shuwairi et al., 2002) and color priming tasks (Jahshan et al., 2012). Therefore, to the best of our knowledge, the present study is the first to elucidate lateralized color search performance and the relationship between target position and color categorical effect in SZ.

The present study revealed two main results: first, patients with SZ showed a significantly slower RT when the target emerged in the RVF than when it emerged in the LVF; and second, regarding the interaction effect of target position and color category, patients with SZ had differential search performance when compared with HCs. In particular, regarding the CP effect, patients with SZ were quicker to detect the target in the LVF than in the RVF when both the target and distractors had different color names. This finding indicates that, in patients with SZ, semantic processing for color name differences influenced visual discrimination performance more greatly in the LVF than in the RVF. However, the same effect was not observed in HCs. These findings suggest that patients with SZ had a different search performance when compared to HCs, which appears to relate to language lateralization in the dominant left hemisphere.

Regarding visual field, several studies have reported asymmetric performance in patients with SZ, such as a slower response in the RVF (Posner et al., 1988; Matsuda et al., 2011) and more omissions in the RVF (Liu et al., 2011), both of which indicate left hemispheric dysfunction. Our results of a significant difference in laterality index show that patients with SZ detected targets more slowly in the RVF than in the LVF and replicated the tendencies for inattention in the RVF reported previously (Posner et al., 1988; Matsuda et al., 2011). The asymmetry of task performances, which suggests left hemispheric dysfunction in SZ, is supported by a visual processing task conducted using either the LVF or RVF (Gur, 1978).

Conversely, the significant visual field difference in CP effect was observed only in the SZ group, indicating a lateralized effect of semantic properties in the color search task in SZ. In patients with SZ, the CP effect, wherein the response of color name difference between the target and distractors was faster in the search task, was observed more strongly in the LVF than in the RVF. In HCs, there was no laterality effect in the current study, which is similar to a previous report by Witzel and Gegenfurtner (2011). The left-lateralized CP effect for color search was also observed in patients with left hemisphere injury (i.e., patients with aphasia) (Paluy et al., 2011). In addition, this laterality effect could vary according to the level of color name acquisition during developmental stages (Franklin et al., 2008). Children who acquired color name showed a right-sided CP effect, whereas children who did not acquire color name showed a left-sided CP effect; the shift in laterality occurred during the process of typical development. Since these findings are relevant to language disintegration in patients with brain-damage and normally developing children, it is suggested that the laterality of the CP effect could be based on plasticity of the brain circuits.

Furthermore, some studies investigated brain activation in HCs who performed a color search task (Liu et al., 2009; Siok et al., 2009). In particular, Siok et al. (2009) suggested that some language regions might play an important role in manipulating top-down control in the color search task. Although the precise mechanism underlying this search performance is unknown, color stimuli could easily activate regions related to color name in the process of detecting the target color. Richter and Zwaan (2009) revealed that the processing of color perception and color naming have overlapping representational resources. This study showed that presentation of a matching color word facilitates quick color discrimination, suggesting that color perception and naming involve similar underlying processes.

A classical study on SZ reported notable descriptions of color categorization (Bolles and Goldstein, 1938). In this study, some patients with SZ refused to classify various shades of green into green color as a whole, indicative of unstable or variant color categorization schema in the brain. In SZ, these findings have been characterized as thought disorder or language disturbances linked to semantic performance (Doughty and Done, 2009). Regarding left hemisphere dysregulation of language, Crow postulated that patients with SZ show different hemispheric specialization for language (Crow, 1997). Crow also suggested that some deterioration, such as semantic deficits, were critical language failures related to hemispheric specialization. Subsequently, Li et al. (2009) suggested that, compared with HCs, left hemisphere dominance of language is generally disturbed in patients with SZ, and that heterogeneity in hemispheric lateralization could underlie psychiatric symptoms. Previous studies regarding language lateralization investigated hemispheric activation with a verbal task, such as a listening task (Koeda et al., 2006; Razafimandimby et al., 2007; Dollfus et al., 2008) or word fluency task (Boksman et al., 2005). Although some studies investigated brain activation using a visual task, such as semantic judgement (Kubicki et al., 2003; Li et al., 2007), only few studies have used semantic tasks with a manipulated visual field. Therefore, further research is needed to investigate the relationship between the lateralized visual task regarding semantic features and brain structure or activation in SZ, which may involve large-scale brain networks related to semantic processing.

Some significant or marginally significant correlations concerning the relationship between search performance and patients’ characteristics were also observed in this study. In particular, the slower RT was related to lower social functioning and more frequent negative and psychopathological symptoms. Furthermore, consistent with the findings of earlier studies, the present study results showed that visual processing was related to functional outcome (Sergi et al., 2006; Rassovsky et al., 2011). Conversely, there was no significant correlation between search performance and chlorpromazine equivalent dose, suggesting that the search performance did not depend on medication use.

Despite the strengths, this study has some limitations. The first limitation is the small sample size. Therefore, in the future, to validate the results of the present study, it is necessary to acquire data with a sufficiently large number of subjects. The second limitation is that we did not confirm the participants’ color blindness by conducting a precise medical evaluation. The finding that all participants performed the color naming task and color search task with high accuracy may, however, preclude such a possibility. Furthermore, this study did not measure eye movement, which might affect search performance.

In conclusion, this study presents two main findings. First, patients with SZ responded more quickly to targets in the LVF than those in the RVF. This laterality effect suggests an advantage for the right hemisphere or disadvantage for the left hemisphere in the visual task in patients with SZ. Second, for patients with SZ, the categorical condition influenced color search performance depending on target position. In the different-category condition, patients with SZ responded more quickly when the target was in the LVF than when it was in the RVF. A similar tendency was not observed in HCs. This lateralized performance could imply failure of left hemisphere dominance in language processing in SZ. A search paradigm combining both the category and target position factors may clarify the mechanism of language in automatic processing and lead to further examination of imbalanced hemispheric function in SZ.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.

This research was approved by the Ethics Committee of Nagoya University School of Medicine (17–604). The patients/participants provided their written informed consent to participate in this study.

TK collected, analyzed and interpreted the data, and wrote the manuscript. TI interpreted the data and also wrote the manuscript. Both authors were involved in drafting the manuscript, reading and approving the final manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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