Effects of pupil size as manipulated through ipRGC activation on visual processing

Abstract

The size of the eyes’ pupils determines how much light enters the eye and also how well this light is focused. Through this route, pupil size shapes the earliest stages of visual processing. Yet causal effects of pupil size on vision are poorly understood and rarely studied. Here we introduce a new way to manipulate pupil size, which relies on activation of intrinsically photosensitive retinal ganglion cells (ipRGCs) to induce sustained pupil constriction. We report the effects of both experimentally induced and spontaneous changes in pupil size on visual processing as measured through EEG. We compare these to the effects of stimulus intensity and covert visual attention, because previous studies have shown that these factors all have comparable effects on some common measures of early visual processing, such as detection performance and steady-state visual evoked potentials; yet it is still unclear whether these are superficial similarities, or rather whether they reflect similar underlying processes. Using a mix of neural-network decoding, ERP analyses, and time-frequency analyses, we find that induced pupil size, spontaneous pupil size, stimulus intensity, and covert visual attention all affect EEG responses, mainly over occipital and parietal electrodes, but—crucially—that they do so in qualitatively different ways. Induced and spontaneous pupil-size changes mainly modulate activity patterns (but not overall power or intertrial coherence) in the high-frequency beta range; this may reflect an effect of pupil size on oculomotor activity and/ or visual processing. In addition, spontaneous (but not induced) pupil size tends to correlate positively with intertrial coherence in the alpha band; this may reflect a non-causal relationship, mediated by arousal. Taken together, our findings suggest that pupil size has qualitatively different effects on visual processing from stimulus intensity and covert visual attention. This shows that pupil size as manipulated through ipRGC activation strongly affects visual processing, and provides concrete starting points for further study of this important yet understudied earliest stage of visual processing.