Identifying the neural origins of pupil constrictions in response to isoluminant stimuli using contrast adaptation

The events causing transient pupil constriction stretch beyond increased illumination. For example, changes in stimulus structure (orientation, color, motion) can cause constriction even if net illumination stays the same. Two explanations for this have been proposed: some argue that altered cortical feature-based responses cause constriction via their input to pupil control nuclei, others argue that local increases in retinal receptor drive a pupil light reflex even if net illuminance does not increase. We tested the two theories using orientation-specific adaptation, which is thought to have a cortical origin. Accordingly, reduced pupil constrictions following orientation-specific adaptation would support a cortical origin of these constrictions. Subjects’ pupil size was recorded while oblique test gratings were presented following presentation of a sliding high-contrast (100%) adapter grating. A test grating’s orientation could be either parallel or orthogonal to that of the adapter that preceded it. In Experiment 1, low-contrast test gratings, with a net luminance equal to that of the background, caused a constriction, but this response was the same for parallel and orthogonal gratings, even though perceptual judgments confirmed the presence of orientation-specific adaptation. In Experiment 2, test contrast was increased to produce more robust constrictions. Still, no orientation-specific modulation was observed. In Experiment 3 we used a test grating in which no pixel had a higher luminance than the background, thus minimizing the possibility of local increases in retinal receptor drive to light reflex. We again observed a transient pupil constriction but no orientation-specific modulation. While our results confirm that the pupil can constrict in response to stimuli that involve no global (Experiments 1-2) or even local (Experiment 3) luminance increases, they do not support the idea that these constrictions reflect altered cortical feature-based responses.