Pupil dilation reflects perceptual selection and predicts subsequent stability in perceptual rivalry

Abstract

During sustained viewing of an ambiguous stimulus, an individual's perceptual experience will generally switch between the different possible alternatives rather than stay fixed on one interpretation (perceptual rivalry). Here, we measured pupil diameter while subjects viewed different ambiguous visual and auditory stimuli. For all stimuli tested, pupil diameter increased just before the reported perceptual switch and the relative amount of dilation before this switch was a significant predictor of the subsequent duration of perceptual stability. These results could not be explained by blink or eye-movement effects, the motor response or stimulus driven changes in retinal input. Because pupil dilation reflects levels of norepinephrine (NE) released from the locus coeruleus (LC), we interpret these results as suggestive that the LC-NE complex may play the same role in perceptual selection as in behavioral decision making.

Fig. 1.

Time course of pupil response. (A) Pupil diameter during Necker cube presentation (40 s from 5 min total) in subject MM. Horizontal lines indicate times of button presses, Necker cube symbols the corresponding percept. Pupil diameter is in arbitrary units (AU) as recorded by the eye-tracker, which are linear in true diameter. For display purposes, diameter is interpolated during blinks (gray). (B–E) Pupil diameter normalized to zero mean and unit standard deviation (z score) and aligned to time of reported switch; mean and SEM. pooled across all switches of all subjects. Black lines denote periods significantly different from 0, at an expected FDR of 0.05 (t test, p < p_FDR=0.05, threshold given in the figure). Insets are visualization aids only and not to scale (B, plaid; c, Structure from Motion (SfM); D, Necker cube; and E, auditory rivalry). (F) Black, All stimuli, representation as in B–E. Green, all stimuli but excluding preswitch durations <3 s (green and black trace overlap exactly for t < −1.5 s, as all analysis truncates traces at the midpoints between switches). (G) All data in normalized time frame (switch at 0, midpoints of dominance durations at ±50%). As z normalization uses absolute time, marker denotes significant difference from the mean of all normalized traces (dashed line).

Fig. 2.

Prediction of dominance durations and control conditions. (A) Significance of the correlation between relative postswitch dominance duration and pupil diameter plotted for each time point ± 3 s around the switch. The logarithmic scale indicates higher significance (lower P values) toward the top. Black, all data from experiment 1; pupil dilation offers the greatest prediction of subsequent perceptual stability 596 ms before the reported switch (r = 0.13, P = 8.5 × 10⁻⁵). Blue, all rivalry data from experiment 2. Red, replay data from experiment 2. The lack of significance in the replay condition shows that the prediction effect is not an artifact of analysis. For experiment 1, where no replay condition exists, this verification is done through surrogate analysis (gray). Horizontal lines indicate the P value thresholds corresponding to an expected FDR of 0.05. (B) Plot of correlation for data of experiment 1 at the time point of peak significance (t = −596 ms). Pink circles mark data from plaid stimulus, which are significant on their own right. (C) Experiment 2 pooled over subjects and stimuli. Red, replay; blue, rivalry. Significance markers for individual thresholds (FDR = 0.05) analogous to Fig. 1. Between the two traces there is no significant difference at any time-point up to an FDR of 0.63; no point after the switch exhibits significance even at an uncorrected 5% level (P > 0.12, for all two-sample t tests). (D) (Upper) Green, z normalized eye-position (distance from center) analyzed analogously to pupil dilation. Black, Pupil dilation trace in same scale for comparison. (Lower) Blink (red) and saccade (blue) frequency compared with pupil diameter trace (black from Fig. 1F). Traces are normalized to the same dynamic range, individual scales are given in the respective color. Data of experiment 1 is used here, but experiment 2 yields comparable results.

Fig. 3.

In the absence of a motor response, average pupil diameter in “counting” is clearly distinguishable for trials with a switch (black) and without switch (cyan). Thin lines denote SEM over trials. Marker denotes periods in which mean traces are significantly different from another at an FDR of 0.1 (no significant points for FDR of 0.05) using two-sample t tests.