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Look away: the anti-saccade task and the voluntary control of eye movement

Abstract

The anti-saccade task has emerged as an important task for investigating the flexible control that we have over behaviour. In this task, participants must suppress the reflexive urge to look at a visual target that appears suddenly in the peripheral visual field and must instead look away from the target in the opposite direction. A crucial step involved in performing this task is the top-down inhibition of a reflexive, automatic saccade. Here, we describe recent neurophysiological evidence demonstrating the presence of this inhibitory function in single-cell activity in the frontal eye fields and superior colliculus. Patients diagnosed with various neurological and/or psychiatric disorders that affect the frontal lobes or basal ganglia find it difficult to suppress the automatic pro-saccade, revealing a deficit in top-down inhibition.

Key Points

  • The anti-saccade task, in which subjects are required to make a saccadic eye movement away from a target, rather than towards it, is a useful task for investigating the voluntary and flexible control of movement. Anti-saccades have a longer latency than pro-saccades and subjects are more likely to make errors on anti-saccade trials. These errors usually consist of a rapid saccade to the target, which is often corrected within a short latency by a second saccade away from the target. Two processes are needed for the anti-saccade task: suppression of the automatic pro-saccade, and inversion of the stimulus vector into the correct saccade vector.

  • Monkeys and humans perform similarly on this task. In electrophysiological studies of monkeys doing the anti-saccade task, saccade neurons in the superior colliculus (SC) and frontal eye fields (FEF) seem to be inhibited before the target appears, to suppress the automatic pro-saccade. This is proposed to prevent activity in these neurons from crossing a threshold that would allow a saccade to be initiated. The suppression could arise from several sources, including other neurons in the FEF and SC, the supplementary eye fields, the dorsolateral prefrontal cortex (DLPFC) and the substantia nigra pars reticulata.

  • The generation of the anti-saccade requires vector inversion and a build-up of activity in a different set of saccade neurons. Monkey electrophysiology studies indicate that vector inversion involves the lateral intraparietal area and/or the FEF.

  • In humans, functional imaging and event-related potential (ERP) studies have been used to study the anti-saccade task. These studies have identified differences in brain activity between pro-saccades and anti-saccades that are consistent with data from electrophysiological studies in monkeys.

  • Young children struggle to perform the anti-saccade task, apparently because they have difficulty in suppressing the automatic pro-saccade. This might relate to the protracted maturation of the frontal lobes, which have been proposed to mediate top-down inhibition of saccade neurons. Patients with lesions of the DLPFC have a similar deficit in performance. By contrast, lesions of the FEF impair the ability of patients to generate the anti-saccade.

  • A number of clinical conditions affect performance on the anti-saccade task. Patients with schizophrenia show increased error rates and prolonged reaction times. Patients with attention-deficit hyperactivity disorder struggle to suppress the automatic pro-saccade but do not show delays in reaction times, whereas those with Parkinson's disease have significantly increased reaction times and also an increased error rate. Tourette's syndrome causes an increase in reaction time with no increase in error rate, possibly because these patients generate increased top-down inhibition as a consequence of adapting to the disorder. All of these findings can be interpreted in the context of an 'accumulator model' of saccade generation.

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Acknowledgements

D.P.M. is supported by the Canadian Institutes of Health Research and the Canada Research Chair Program. S.E. is supported by the National Alliance for Research on Schizophrenia and Depression, CIHR and the EJLB Foundation. J. Fecteau and J. Connolly commented on an earlier version of the manuscript.

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The authors declare no competing financial interests.

Correspondence to Douglas P. Munoz.

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Glossary

SACCADIC EYE MOVEMENT

A rapid eye movement (with speeds of up to 800 degrees per second) that brings the point of maximal visual acuity — the fovea — to the image of interest.

VISUAL GRASP REFLEX

Flexive orienting response towards a novel visual stimulus.

FRONTAL EYE FIELD

An area in the frontal lobe that receives visual inputs and produces movements of the eye.

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Figure 1: The anti-saccade task.
Figure 2: Discharges recorded from a fixation neuron (FN) and a saccade neuron (SN) in frontal eye field and superior colliculus when a monkey performs the pro-saccade and anti-saccade tasks in the gap condition.
Figure 3: Activity of individual saccade neurons in the frontal eye field and superior colliculus.
Figure 4: An accumulator model can be used to represent the accumulation of saccade activity in the brain on anti-saccade trials.