Abstract
The pupil provides a rich, non-invasive measure of the neural bases of perception and cognition and has been of particular value in uncovering the role of arousal-linked neuromodulation, which alters both cortical processing and pupil size. But pupil size is subject to a multitude of influences, which complicates unique interpretation. We measured pupils of observers experiencing perceptual multistability-an ever-changing subjective percept in the face of unchanging but inconclusive sensory input. In separate conditions, the endogenously generated perceptual changes were either task-relevant or not, allowing a separation between perception-related and task-related pupil signals. Perceptual changes were marked by a complex pupil response that could be decomposed into two components: a dilation tied to task execution and plausibly indicative of an arousal-linked noradrenaline surge, and an overlapping constriction tied to the perceptual transient and plausibly a marker of altered visual cortical representation. Constriction, but not dilation, amplitude systematically depended on the time interval between perceptual changes, possibly providing an overt index of neural adaptation. These results show that the pupil provides a simultaneous reading on interacting but dissociable neural processes during perceptual multistability, and suggest that arousal-linked neuromodulator release shapes action but not perception in these circumstances.
Highlights
The brainstem’s neuromodulatory systems can profoundly influence cognitive functions by altering neural response properties within the cortical circuits that mediate those functions (Aston-Jones and Cohen, 2005; Sara and Bouret, 2012; Lee and Dan, 2012; Pfeffer et al, 2018)
We further found that these two response components differ in their relationship to the timing of the perceptual sequence. It is the perception-related constriction, rather than the reportrelated dilation, that shows a robust dependence on this timing. These results indicate that pupil signals during perceptual multistability include two overlapping but separable components: both a dilation that is plausibly related to arousal-linked noradrenaline release at a physiological level and to task execution at a behavioral level, and a constriction that accompanies visual cortical processes closely tied to perception
The application of pupillometry methods in the context of multistable perception holds promise as an approach to studying perception and its neuromodulatory dependencies, both because the pupil non-invasively informs about transient noradrenergic activity accompanying perceptual switches, and because such activity may be reflected, on a slower timescale, in the spontaneous dynamics of the perceptual cycle
Summary
The brainstem’s neuromodulatory systems can profoundly influence cognitive functions by altering neural response properties within the cortical circuits that mediate those functions (Aston-Jones and Cohen, 2005; Sara and Bouret, 2012; Lee and Dan, 2012; Pfeffer et al, 2018). Recent work has used multistable visual stimuli to examine neuromodulatory influences on visual processing Such stimuli cause perception to alternate between different interpretations of the sensory data, and recent work suggests that the noradrenergic arousal system associated with the brainstem’s locus coeruleus impacts perception in this situation, perhaps by altering the response gain of visual cortical neurons involved (Einhauser et al, 2008; Sara and Bouret, 2012; Laeng et al, 2012; Kloosterman et al, 2015a; Pfeffer et al, 2018).
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