The tell-tale tasks: A review of saccadic research in psychiatric patient populations
Introduction
The saccadic eye movement system is responsible for rapid eye movements that bring the image of an object onto the fovea (see glossary) (Leigh & Zee, 1983). Saccades are conjugate, ballistic eye movements that are characterized by short reaction times, typically around 200 ms, and brief durations, normally between approximately 20 and 120 ms (Engelken et al., 1989, Gouras, 1985, Leigh and Zee, 1983). In humans, saccades can reach speeds of up to 600–700 deg/s, whereas monkeys can produce saccades that are nearly twice as fast (De Renzi, 1988, Gouras, 1985). Normal saccadic eye movements are characterized by an invariant relationship between their peak velocity and their size; the amplitude–peak velocity relationship is referred to as the main sequence (Bahill, Clark, & Stark, 1975).
Accuracy of saccades depends on the location of a target on the retina as well as the position of the eyes in the orbit (Gouras, 1985). There are two major classes of saccades, namely, those that are externally triggered and automatic, and those that are internally initiated and volitional (Lasker, Zee, Hain, Folstein, & Singer, 1987). Although saccadic eye movements are typically elicited by the sudden appearance of a novel auditory or visual stimulus that attracts the subject’s attention (reflexive saccades), they can be produced on command, in the dark, to remembered targets, during scanning or searching of stationary visual scenes, or with closed eyes (De Renzi, 1988, Gouras, 1985, Leigh and Zee, 1983, Wirtschafter and Weingarden, 1988). Saccades can be described in terms of their reaction time, namely, the time elapsing from the command signal to shift one’s gaze until the beginning of the saccade. Saccades are also described in terms of their velocity and accuracy.
Diefendorf and Dodge (1908) were the first investigators to report on the functioning of the saccadic system in schizophrenia patients. Since then, interest in the study of saccadic eye movements in schizophrenia has risen steadily and now includes a focus on volitional saccades as well as reflexive ones. Saccadic eye movements can be measured reliably and precisely. As a result of basic research including single unit recordings and lesion studies as well as clinical research and functional imaging, there is a considerable body of knowledge regarding the neurophysiology of the saccadic eye movement subsystem. Thus, the study of saccadic eye movements in psychiatric patient groups can provide a “window into the brain” of affected individuals. Over the past three decades, there has also been an increase in the number of studies of saccadic performance in other psychiatric patient groups. Much of the impetus for the focus on saccadic eye movements in these populations comes from the fact that saccades provide a non-invasive yet accessible means of investigating psychomotor functioning as well as higher-order cognitive processes and their underlying neural mechanisms.
In the following review, we summarize the extant literature regarding the study of saccadic eye movements in adult psychiatric patients. In order to appreciate the growing complexity of the area and the various ways in which psychiatric patient groups differ in terms of their saccadic task performance, we introduce the major saccadic paradigms prior to summarizing the studies for each diagnostic group. Given the disproportionately large corpus of literature on saccadic performance in schizophrenia and schizophrenia-spectrum populations, this area will receive particular emphasis in our review. Findings regarding the symptom, neurocognitive, and neural correlates of saccadic performance, as well as hypotheses regarding the functional significance of patients’ saccadic deficits are also discussed. In the final section of the review, we integrate across findings, and provide a comparative analysis of saccadic deficits in the different psychiatric disorders. This discussion is used as an opportunity for hypothesis generation and recommendations for future directions.
Section snippets
Different types of saccade paradigms
Because of the versatility of saccades, a number of different behavioral tasks have been developed over the years to probe different underlying mechanisms. Below we review some of the most commonly used saccadic eye movement tasks. The different saccade tasks include visually-guided, memory-guided, gap, overlap, and antisaccade tasks. Each task has different demands allowing for the assessment of the integrity of brain pathways in health and disease. For example, to assess the integrity of
Saccadic performance in schizophrenia and schizophrenia-spectrum disorders
Most of the studies of saccadic performance in psychiatric samples have focused on schizophrenia patients. Additionally, several studies have investigated performance on saccadic tasks in schizophrenia-spectrum populations such as schizotypal personality disorder and/or individuals at heightened risk for the later development of schizophrenia and schizophrenia-spectrum disorders. In this review, studies focusing on schizophrenic patient samples will be addressed first prior to discussing the
Performance on Memory-Guided (Oculomotor Delayed-Response) Tasks
Schizophrenia patients’ oculomotor delayed-response task performance is characterized by excessive anticipatory saccades during the delay-period (Camchong et al., 2006, Everling et al., 1996, Hommer et al., 1991, Landgraf et al., 2008, McDowell and Clementz, 1996, McDowell et al., 2001, Park, 1997, Park and Holzman, 1992). In memory-guided saccades, schizophrenia patients typically display increased latencies and/or decreased gain (Everling et al., 1996, Landgraf et al., 2008, McDowell and
Schizophrenia patients’ performance on scanpaths and visual search tasks
When subjects were required to use visuospatial cues (arrows) to guide their sequence of scanning, Reischies, Stieglitz, Mielewczyk, and Vogel (1989) observed that schizophrenia patients produced a higher number of errors and displayed increased saccadic latency, relative to normals. When Gaebel, Ulrich, and Frick (1987) examined the visuomotor performance of partially remitted schizophrenia patients in a picture viewing task, they found two subgroups of patients who displayed opposite scanning
Neural correlates of saccadic performance in schizophrenia
In humans,1 evidence from functional imaging studies (Melamed & Larsen 1979), electrophysiological studies (Evdokomidis et al., 1996, Klein, Brugner et al., 2000, Klein, Heinks et al., 2000), lesion studies (Gooding et al., 1999,
Possible mechanisms underlying antisaccade task deficits in schizophrenia patients
There have been several interpretations of schizophrenia patients’ antisaccade task deficits. In the following section, we summarize various research efforts to identify mechanisms underlying the observed impairments. Perhaps the most parsimonious interpretation of patients’ antisaccade deficits is that they reflect a general oculomotor deficit. However, given schizophrenia patients’ ability to perform within normal limits on simple saccadic refixation tasks, their abnormal performance on
Saccadic performance in other psychiatric patient populations
An increasing number of studies have addressed saccadic performance in other psychiatric patient populations. In the next section, findings from these studies will be reviewed. Data regarding comparisons between other psychiatric patient groups and schizophrenia patients will be discussed as well.
Saccadic performance in ADHD
Relatively few investigations of saccadic performance in attention deficit hyperactivity disorder (ADHD) examine adults. Error rates in prosaccade tasks are similar across ADHD patients and healthy control populations (Carr et al., 2006, Feifel et al., 2004, Munoz et al., 2003). Findings regarding saccadic latency differences between ADHD patients and healthy controls vary. For example, Munoz et al. (2003) found that the latency of visually-guided prosaccades is longer and more variable in
Saccadic performance in Tourette’s Syndrome
Research on saccadic performance in individuals with Tourette’s Syndrome (TS) is relatively sparse. Data suggest that TS patients’ reflexive prosaccade reaction times are normal or only slightly elevated (Farber et al., 1999, Straube et al., 1997) and their saccadic durations are shorter (Farber et al., 1999). During a prosaccade gap task, Farber et al. (1999) noted that patients with TS showed more anticipatory saccades, though they did not differ from healthy controls in terms of the
Saccadic performance in obsessive compulsive disorder
There is a small but growing body of research that focuses on gaze fixation abnormalities in phobic patients (see Bar-Haim, Lamy, Pergamin, Bakermans-Kranenburg, & van IJenzdoorn, 2007 for a recent review). In one intriguing study, social phobia patients displayed markedly different scanpath patterns, including reduced scanning of the interpersonal (facial expression) stimuli and fewer fixations to salient facial features (Horley, Williams, Gonsalvez, & Gordon, 2003). Overall, there has not
Discussion
This review illustrates the growing number of investigations of saccadic eye movements in adult psychiatric patients. A variety of oculomotor tasks designed to assess reflexive and volitional saccades have been administered in the hopes of discerning more about the processes that are impacted by the mental disorders and the pathophysiological mechanisms by which these processes are disrupted. In this section, we attempt to summarize findings across the disorders, and highlight the similarities
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