Reward and Efficacy Modulate the Rate of Anticipatory Pupil Dilation

Abstract

Pupil size is a well-established marker of cognitive effort, with greater efforts leading to larger pupils. This is particularly true for pupil size during task performance, whereas findings on anticipatory effort triggered by a cue stimulus are less consistent. For example, a recent report by Frömer et al. found that in a cued-Stroop task, behavioral performance and electrophysiological markers of preparatory effort allocation were modulated by cued reward and 'efficacy' (the degree to which rewards depended on good performance), but pupil size did not show a comparable pattern. Here, we conceptually replicated this study, employing an alternative approach to the pupillometry analyses. In line with previous findings, we found no modulation of absolute pupil size in the cue-to-target interval. Instead, we observed a significant difference in the rate of pupil dilation in anticipation of the target: pupils dilated more rapidly for high-reward trials in which rewards depended on good performance. This was followed by a significant difference in absolute pupil size within the first hundreds of milliseconds following Stroop stimulus onset, likely reflecting a lagging effect of anticipatory effort allocation. Finally, the slope of pupil dilation was significantly correlated with behavioral response times, and this association was strongest for the high-reward, high-efficacy trials, further supporting that the rate of anticipatory pupil dilation reflects anticipatory effort. We conclude that pupil size is modulated by anticipatory effort, but in a highly temporally-specific manner, which is best reflected by the rate of dilation in the moments just prior to stimulus onset.

Keywords: efficacy; effort; preparatory control; pupillometry; reward.

FIGURE 1

Experiment stimuli (A) and trial structure (B). For cue stimuli (A), gray always indicated ‘low’ reward and/or efficacy, while cyan and magenta ‘hands’ and ‘bags’ indicated ‘high’ reward and/or efficacy. The side of the screen on which the hand or bag was presented was constant for a given participant but counterbalanced between participants, as was the color coding for reward and efficacy. For each trial (B) all Stroop stimuli were incongruent (different word meaning and ink color; “GEEL” is the Dutch word for “YELLOW”); an ITI of 1500–2500 ms occurred between trials in which only the fixation cross was presented onscreen.

FIGURE 2

Mean, baseline‐corrected pupil size and t‐values for the post‐cue and post‐Stroop time‐windows of interest. Top left panel represents the mean, baseline‐corrected pupil size (pixels) during the cue‐to‐target interval; top right panel represents mean, baseline‐corrected pupil size following the Stroop stimulus; lower panels represent t‐value time‐course for comparisons of mean pupil size in sequential 50 ms bins for the cue‐to‐target interval (bottom left) and following the Stroop stimulus (bottom right). Solid vertical lines represent stimulus onset times; dashed, black horizontal lines indicate the p = 0.05 significance threshold; solid horizontal lines in the lower portion of the bottom right panel indicate t‐values which survive FDR correction for multiple comparisons.

FIGURE 3

Mean response accuracy (left) and response times (right) in the Stroop task, error bars represent ±1 SE corrected for within subjects differences (Cousineau 2005).

FIGURE 4

Scatterplots of the correlation between average RT and pupil dilation slopes for each experimental condition.

FIGURE 5

Average pupil size (A), linear fit to pupil size (B), and slope of the linear fits (C) within the time window from 700 ms before until 300 ms after the Stroop stimulus onset.