The pupil reflects motor preparation for saccades – even before the eye starts to move

Stephanie Jainta

doi:10.3389/fnhum.2011.00097

Abstract

The eye produces saccadic eye movements whose reaction times are perhaps the shortest in humans. Saccade latencies reflect ongoing cortical processing and, generally, shorter latencies are supposed to reflect advanced motor preparation. The dilation of the eye’s pupil is reported to reflect cortical processing as well. Eight participants made saccades in a gap and overlap paradigm (in pure and mixed blocks), which we used in order to produce a variety of different saccade latencies. Saccades and pupil size were measured with the EyeLink II. The pattern in pupil dilation resembled that of a gap effect: for gap blocks, pupil dilations were larger compared to overlap blocks; mixing gap and overlap trials reduced the pupil dilation for gap trials thereby inducing a switching cost. Furthermore, saccade latencies across all tasks predicted the magnitude of pupil dilations post hoc: the longer the saccade latency the smaller the pupil dilation before the eye actually began to move. In accordance with observations for manual responses, we conclude that pupil dilations prior to saccade execution reflect advanced motor preparations and therefore provide valid indicator qualities for ongoing cortical processes.

Highlights

The regulation of pupil size is a result of a complex interrelationship between the parasympathetic and sympathetic pathways of the human autonomic nervous system
Mixing gap and overlap rendered the latency for gap trials similar to those in overlap trials; we found only marginally shorter latencies for gap trials (200 ± 16.9) than for overlap trials (207 ± 22.5) in mixed blocks, on average
Further (b) mixing gap and overlap trials showed switching costs, i.e., saccade latencies increased for gap trials. (c) Pupil dilations prior to saccade execution were larger for gap than for overlap tasks and switching costs were present in the pupil data. (d) Saccade latencies across different gap and overlap tasks significantly affect pupil dilation prior to the eye movement’s execution

Summary

Introduction

The regulation of pupil size is a result of a complex interrelationship between the parasympathetic and sympathetic pathways of the human autonomic nervous system. Pupil constrictions or dilations mainly regulate the amount of light entering the eye (Lowenstein and Loewenstein, 1969) Besides this basic function, the observation of the dilation of the eye’s pupil has a long history and well-described potential to help uncover cortical and subcortical processing activity (Hess and Howell, 1988; Beatty and Brennis, 2000; Wilhelm et al, 2002; Porter et al, 2007; Conway et al, 2008). Karatekin et al (2010) reported a comparison between a pro- and anti-saccade task; in an anti-saccade task participants are presented with a visual target on one side of a fixation dot but instructed to look away from it, i.e., they are instructed to make a saccade toward a blank location on the opposite side of the screen This anti-saccade task produced longer latencies when compared to the pro-saccade task, and in parallel, absolute pupil diameters increased for anti-saccades. We were led to believe that if the pupil response could directly reflect motor preparations it might appear within other standard paradigms involving saccade execution as well

Methods

Results

Conclusion