Pupil size is sensitive to stimulus features independent of effects of arousal

Abstract

Aside from luminance, pupil size is modulated by stimulus properties such as contrast and spatial frequency. Additionally, pupil size is affected by cognitive processes, including attention and arousal. However, it's unclear how these factors interact with each other. We hypothesized that stimulus properties interact, independent from arousal effects on pupil size. We measured pupil responses to equiluminant stimuli and tested how response amplitude depends on contrast, spatial frequency, and reward. Pupil size was recorded in 65 subjects (20,723 trials total) performing a demanding RSVP task at fixation, while attention and mean luminance were kept constant. High and low levels of reward modulated arousal. On 75% of trials, task-irrelevant stimuli appeared in the periphery. These stimuli consisted of sinusoidal gratings at two different contrast levels and five different spatial frequencies. On the remaining trials (null) no gratings appeared. Modulation in pupil response on null trials was hence attributable solely to the cognitive aspects of the task. To estimate task-related pupil responses, we modeled responses on stimulus trials as a combination of task-related and stimulus-evoked components and then regressed against the mean response to obtain trial-wise amplitude estimates. On null trials, the pupil size increased following trial onsets. These task-related responses were larger on high reward trials, indicating that reward modulated arousal, as expected. Stimulus-evoked responses, however, were unaffected by reward level. Stimulus-evoked response amplitude increased with contrast and with spatial frequency. We further uncovered an interaction between contrast and spatial frequency; the effect of spatial frequency was larger for high than for low contrast. Our results shed light on interactions between pupillary response pathways. Specifically, under constant luminance, unattended stimuli evoke responses that are distinct from general arousal or attentional effects. Finally, future studies should account for effects of stimulus properties in order to correctly identify impact of higher cognitive processes.