Visual scanning deficits in schizophrenia and their relationship to executive functioning impairment

Abstract

Abnormal visual scanning of faces, objects, and line drawings has been observed in patients with schizophrenia and is thought to reflect neurocognitive impairment. In this study, a simultaneous measurement approach was used to assess whether schizophrenia patients demonstrate restricted visual scanning when confronted with a complex problem-solving stimulus, and whether visual scanning deficits are predictive of inflexible thinking. Thirty-eight schizophrenia patients and 30 comparison participants were presented with Rorschach inkblots while eye movements were monitored and verbal responses to the stimuli were recorded and scored for inflexible thinking using the Rorschach Repetition and Perseveration Scale. Schizophrenia patients demonstrated fewer and longer visual fixations and shorter total scanpath relative to comparison participants but did not differ on mean scanpath length. Among patients, fewer fixations were associated with a higher frequency of verbal perseverations. Correlations between scanning measures and symptoms showed that negative symptoms were related to a minimal scanning or “staring” approach. Results support previous findings of restricted visual scanning in schizophrenia patients, are consistent with previously observed relationships between visual scanning and symptom profiles, and suggest that visual organizational deficits during complex problem-solving tasks may be related to cognitive inflexibility and frontal-executive dysfunction.

Introduction

Visual scanning and eye movements provide information about how visual stimuli are internally represented (Noton and Stark, 1971). As the eyes move and the retina fixates on novel and salient stimulus features, important information in the environment is identified. Visual scanpaths provide a “real-time” and a high-resolution index of the cognitive processing of visual information (Manor et al., 1999). Incoming visual signals progress through a complex neural circuit that includes the frontal eye fields and association regions such as the dorsolateral prefrontal cortex (DLPFC). The relationship between visual scanning and higher order cognition is illustrated by the evidence that brain areas responsible for executive functions, such as the DLPFC, are activated when humans generate eye movements to locations of interest (Leigh and Zee, 1999).

Visual scanning abnormalities in patients with schizophrenia have been observed across a range of visual stimuli, including simple geometric figures (Kojima et al., 1992, Matsushima et al., 1992, Obayashi et al., 2003), faces (Gordon et al., 1992, Loughland et al., 2002, Manor et al., 1999, Phillips and David, 1997, Streit et al., 1997, Williams et al., 1999), and line drawings (Gaebel et al., 1987, Kurachi et al., 1994). Specifically, patients with schizophrenia have shorter scanpath lengths (the distance the eyes move between fixations), longer duration of fixations, and fewer fixations on important features of a visual stimulus. Collectively, the findings from these studies suggest that that the more restricted visual search strategy of schizophrenia patients reflects the reduced processing of salient visual information. Restricted visual scanning of faces during facial affect recognition tasks, for example, may indicate impairments in social cognition and may be a trait-related vulnerability marker of the illness (Loughland et al., 2002, Loughland et al., 2004). While authors have speculated about the relevance of visual scanning deficits to neurocognitive impairment, the relationship between restricted visual scanning and other measures of cognitive functioning has been relatively unexplored.

The underlying etiology of visual scanning deficits in schizophrenia is relatively unknown (Manor et al., 1999); however, it has been suggested that frontal lobe pathology may be involved (McDowell et al., 1996). The frontal lobes are thought to be responsible for higher order executive functions such as the solving of complex problems and adjusting behavior appropriately in response to changes in the environment (Damasio and Anderson, 1993). If impaired frontal lobe functioning underlies visual scanning abnormalities in schizophrenia, it is reasonable to hypothesize that visual scanning deficits in this population would be observed in response to a complex and visually ambiguous problem-solving task, along with other apparent markers of frontal lobe dysfunction. For example, perseverative behavior, defined as unintentional, repetitive behavior that is influenced by a previous response and may be inappropriate to current environmental demands (Crider, 1997), is thought to reflect abnormalities in frontal-executive functioning (Levin, 1984) and has previously been linked to increased negative symptoms, as well as cognitive deficits during complex problem-solving situations (Perry et al., 1998).

The majority of research on visual scanning deficits in schizophrenia has used identification tasks using familiar stimuli, such as faces; yet, it has been recognized that the use of more novel and ambiguous stimuli is warranted (Phillips and David, 1997). The results of visual scanning studies with face stimuli have been largely interpreted to suggest that schizophrenia patients have prominent deficits in social awareness and interpersonal communication. The perception of faces is thought to be highly practiced and automatic and theoretically elicits mostly “gestalt” or holistic processing (Haxby et al., 2000, Maurer et al., 2002) but also requires detailed local analysis to make subtle discriminations. Therefore, previous findings provide a basis for generating hypotheses as to how schizophrenia patients will scan novel and complex stimuli that require both holistic and detail-based perceptions. A highly engaging and challenging visual task will theoretically tax schizophrenia patients' limited capacity for complex problem solving. It then becomes possible to assess whether visual scanning deficits are related to a breakdown in the ability to respond appropriately according to task demands and result in an inflexibility of thinking and behavior (e.g., perseverative behavior) in response to the task.

One aim of the current study was to examine whether schizophrenia patients evidence visual scanning deficits during the presentation of a novel and complex problem-solving task, the Rorschach Test, which requires the subject to process unfamiliar, ambiguous stimuli and provide a cohesive and organized response. An additional aim was to assess whether visual scanning abnormalities in schizophrenia are associated with frontal-executive functioning deficits, as reflected by verbal perseverations. To better understand the relationship between two domains of brain functioning, it is important to obtain measures in close temporal proximity because cognitive processing is dynamic and fluctuates over time with changes in task demand, state variables, and a number of other factors (Gjerde, 1983, Perry et al., 1999). Therefore, we used a simultaneous approach where visual scanning of the Rorschach stimuli was measured in close temporal proximity with verbal output that was scored for perseverations. We hypothesized that, consistent with previous literature, patients with schizophrenia would show reduced visual fixations, increased duration of fixations, and short scanpath lengths, suggesting that they are impaired in the ability to organize and process complex visual information. Furthermore, we hypothesized that restricted visual scanning of complex stimuli would be associated with increased verbal perseverations.