Separable pupillary signatures of perception and action during perceptual multistability

  1. Jan W Brascamp
  2. Gilles de Hollander
  3. Michael D Wertheimer
  4. Ashley N DePew
  5. Tomas Knapen

  • Curated by eLife

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    Evaluation Summary:

    Pupillometry is an increasingly accessible tool for the non-invasive readout of brain activity. However, our understanding of pupil-control circuits and of the relationship between changes in pupil size and perception, cognition or action is incomplete. Therefore, any measurements that further this understanding are of great interest to a wide audience in psychology and neurobiology. This study used pupillometry to explore the neural processing underlying perception and dissociate them from action-related neural processing. Results reveal changes in pupil size that are reliably different depending on the task. Such approaches can be very useful in deciphering which of the myriad factors that can affect pupil size are active under specific, controlled conditions.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer 3 agreed to share their names with the authors.)

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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.

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  1. Version published to 10.7554/elife.66161 on eLife
  2. eLife

    Reviewer #3 (Public Review):

    The authors investigated pupillary response looking at the changes corresponding to perceptual events (spontaneous or physical changes) and contrasting them with requirements of over reporting (changes were reported or ignored). They demonstrate that the former is associated with a rapid constriction and re-dilation, whereas the latter shows an opposite effect with dilation being followed by re-constriction. The particular strength of the work is in no-report conditions using on OKN-based inference about timing of perceptual events that allowed for this dissociation to be observed, whereas manual report conditions allowed for a direct comparison with prior work. The analysis and control experiments are very thorough showing that reported results are unlikely to be explained other factors such as saccades or blinks.

    The study makes a significant contribution but proposing a no-report paradigm for identifying perceptual events that should work for any multistable display. The fairly rapid pupil constriction event could provide an easy to detect and temporally reliable marker of perceptual switches, expanding ways the multistability data is collected. The same approach could also be useful for no-report studies of visual awareness in general.

    The ability to decompose pupillary response into two components - perception and over manual response - will also be useful for studying neural correlates of spontaneous perceptual switches, as it could help to better understand switch-time activity in various frontal and parietal regions. Here, also some regions are associated with active response, whereas other with perception, distinction that could be potentially better understood based on the idea that only the former involves noradrenaline-affected processing. My main worry methodologically is the under and overestimation of mean switch rate via OKN (figure 1C). OKN estimates are all within .4-.8 range, whereas for self-report rates differ from 0.2 to over 1. Further analysis would be helpful. I think it would be helpful if the authors elaborated on what kind of switches went unreported (or, conversely, what kind of events led to false alarms): switches before very short dominance phases (could be to fast to report via key presses), to return transitions, etc.

  3. eLife

    Reviewer #2 (Public Review):

    Pupillometry is an increasingly accessible tool for the non-invasive readout of brain activity. However, our understanding of pupil-control circuits and of the relationship between changes in pupil size and perception, cognition or action, is far from complete. Therefore, any measurements that further this understanding are of great interest to a wide audience in the field of psychology and neurobiology.

    This study used pupillometry to explore the neural processing that underlie perception and dissociate those from action-related neural processing. The authors use a novel and comprehensive task design, centered on binocular rivlary, that is likely to find wider use among researchers studying the neural processes that underlie perception and action. They used a non-invasive method (pupillometry) to disscociate putative processes and circuits that might drive perceptual switching. They found changes in pupil size that are reliably different depending on the task: for example - between the conditions that require reporting a perceptual switch versus not reporting it and between rivalrous and explicit changes in the visual stimulus.

    Such approaches can be very useful in deciphering which of the myriad factors that can affect pupil size are in fact active under specific, controlled conditions and thus provide a basis for guided, direct measurements of these specific brain regions.

    Overall, this study is well-conceived and executed. However, I have some questions and concerns about the analyses and conclusions made from the results shown. In general, I would encourage the authors to try and include more of what we do know about neuromodulation and the cortical control of pupil pathways to frame the hypothesis and interpret the results. Further, it is unclear to me whether the constriction/dilation dissociation is tenable with the presented data and analyses.

  4. eLife

    Reviewer #1 (Public Review):

    Brascamp and colleagues address pupil-size changes around perceptual switches in perceptual multistability. Several previous studies have found pupil dilation around or after the switch and some have found pupil constriction, though the latter was typically less robust. Moreover, while most previous studies included some controls for the effect of reporting and for the physical stimulus change, to my knowledge, so far, no study has fully crossed the factors report/no-report and endogenous/exogeneous switch. In the present study, this gap is filled using a binocular-rivalry stimulus and an OKN-based no-report paradigm. This allows the authors to isolate the constriction component from the dilation component and interestingly they find the constriction more robustly tied to the perceptual switch, while the dilation component is mostly related to the response. Experiments are soundly conducted and analysed and results are interpreted with appropriate care. Since the results challenge frequent interpretations as to why perceptual switches in multistability may cause pupil-size changes, the paper is of high relevance to the fields of pupillometry and multistability, but also to other areas where pupillometry is used as index of perceptual and cognitive processes. I only have some minor questions and requests for clarification with regard to result presentation and interpretation.

  5. eLife

    Evaluation Summary:

    Pupillometry is an increasingly accessible tool for the non-invasive readout of brain activity. However, our understanding of pupil-control circuits and of the relationship between changes in pupil size and perception, cognition or action is incomplete. Therefore, any measurements that further this understanding are of great interest to a wide audience in psychology and neurobiology. This study used pupillometry to explore the neural processing underlying perception and dissociate them from action-related neural processing. Results reveal changes in pupil size that are reliably different depending on the task. Such approaches can be very useful in deciphering which of the myriad factors that can affect pupil size are active under specific, controlled conditions.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer 3 agreed to share their names with the authors.)

  6. Version published to 10.1101/2021.01.22.427816v1 on bioRxiv