Dissociable saccadic suppression of pupillary and perceptual responses to light

Abstract

We measured pupillary constrictions in response to full-screen flashes of variable luminance, occurring either at the onset of a saccadic eye movement or well before/after it. A large fraction of perisaccadic flashes were undetectable to the subjects, consistent with saccadic suppression of visual sensitivity. Likewise, pupillary responses to perisaccadic flashes were strongly suppressed. However, the two phenomena appear to be dissociable. Across subjects and luminance levels of the flash stimulus, there were cases in which conscious perception of the flash was completely depleted yet the pupillary response was clearly present, as well as cases in which the opposite occurred. On one hand, the fact that pupillary light responses are subject to saccadic suppression reinforces evidence that this is not a simple reflex but depends on the integration of retinal illumination with complex "extraretinal" cues. On the other hand, the relative independence of pupillary and perceptual responses suggests that suppression acts separately on these systems-consistent with the idea of multiple visual pathways that are differentially affected by saccades.

Keywords: parallel visual pathways; perisaccadic suppression; pupil; pupillary light reflex; saccadic eye movements; vision for action.

Fig. 1.

Methods. A: stimulus and task. Subjects made saccades from the fixation point to the saccade target (red points), as illustrated by the arrow (not part of the display). The flash stimulus was a full-field luminance increment, lasting 1 monitor frame. B: timing of the flash relative to the saccade. Except in catch trials where it was not presented, the flash could occur perisaccadically (immediately upon online saccade onset detection), 500 ms postsaccadically, or ∼500 ms presaccadically. C–E: saccade parameters (latency, amplitude and peak velocity) in the 4 conditions, averaged across trials and subjects. Presaccadic flashes tend to interfere with saccade planning, resulting in slightly delayed and larger saccades with significantly lower peak velocity, but saccade parameters were all well matched across the other conditions. Asterisk marks only significant difference (P < 0.05) between no-flash condition (black) and other conditions (color-coded as in B).

Fig. 2.

Pupillary traces. Pupil size change as a function of time from saccade onset, plotted separately for trials in which the flash occurred before/during/after the saccade or was withheld (different colors) and for the different luminance levels of the flash (y-offset; luminance as shown). Traces are averages across all trials from all subjects (with thin lines giving 95% confidence intervals), computed after subtracting from each trial the mean pupil size in the first 500 ms (A) and subtracting the average pupil trace in the saccade-only condition from each subject and experimental session (B). Black dashed lines mark 0 for each group of traces; triangles in x-axis mark the time of flash presentation. Scale is the same in A and B (shown in B, top).

Fig. 3.

Suppression of light responses. A and B: peak pupil response (i.e., minimum of pupil traces in Fig. 2, A and B, respectively) as a function of flash luminance, with black lines giving the response in the saccade-only (no flash) condition. Symbols and thick lines give the grand average across trials from all subjects, and thin lines give 95% confidence intervals. C: proportion of trials where the flash was reported as seen. The line gives the best-fit cumulative Gaussian function across the aggregate data from all subjects (symbols). See Fig. 4 for individual psychometric functions. D: pupillary response (same conventions as in B), computed separately for perisaccadic flashes that were reported as seen or as unseen.

Fig. 4.

Suppression of individual light responses. A: individual suppression indexes, computed as the difference between the detection rate or the pupillary response observed for perisaccadic flashes and the same responses for postsaccadic (left) or presaccadic (right) flashes. Subjects are ordered based on the suppression of detection rate; the same order and color coding is used in Fig. 5. Error bars are SE of the difference, computed from the SE of the means of the 2 conditions considering the propagation of errors. *P < 0.05; ns, nonsignificant. B and C: average detection rate (B) and pupillary response (C) for perisaccadic flashes, plotted as a function of the exact flash time relative to the saccade onset (means in continuous nonoverlapping 5-ms bins) and shown separately for the different flash luminance levels (grayscale: highest luminance in white and lowest in dark gray). Error bars are SE; data pooled across subjects.

Fig. 5.

Responses to perisaccadic seen and unseen flashes. A: individual psychometric curves plotting, for each subject (color-coded, preserved across the 3 panels), the proportion of seen perisaccadic flashes against their luminance (symbols with error bars showing SE across trials) and the best-fit cumulative Gaussian function across the data. B: pupillary response to perisaccadic flashes (computed as in Fig. 3B). C: Spearman rank correlation between luminance of the flash and the seen/unseen report or the amplitude of the pupillary response (significant for most subjects; *P < 0.05), and partial correlation between the seen/unseen report and the pupillary response after controlling for the effect of luminance [nonsignificant (ns) with P > 0.05 in all but 1 subject]. Bars on right display the number of trials considered for these correlations. Error bars report SE of the correlation coefficient, computed as SE = √[(1 − r²)/(n − 2)].