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A dynamic sequence of visual processing initiated by gaze shifts

View ORCID ProfilePhilip R. L. Parker, View ORCID ProfileDylan M. Martins, View ORCID ProfileEmmalyn S. P. Leonard, Nathan M. Casey, View ORCID ProfileShelby L. Sharp, View ORCID ProfileElliott T. T. Abe, View ORCID ProfileMatthew C. Smear, View ORCID ProfileJacob L. Yates, View ORCID ProfileJude F. Mitchell, View ORCID ProfileCristopher M. Niell
doi: https://doi.org/10.1101/2022.08.23.504847
Philip R. L. Parker
1Institute of Neuroscience and Department of Biology, University of Oregon, USA
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Dylan M. Martins
1Institute of Neuroscience and Department of Biology, University of Oregon, USA
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Emmalyn S. P. Leonard
1Institute of Neuroscience and Department of Biology, University of Oregon, USA
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Nathan M. Casey
1Institute of Neuroscience and Department of Biology, University of Oregon, USA
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Shelby L. Sharp
1Institute of Neuroscience and Department of Biology, University of Oregon, USA
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Elliott T. T. Abe
1Institute of Neuroscience and Department of Biology, University of Oregon, USA
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Matthew C. Smear
2Institute of Neuroscience and Department of Psychology, University of Oregon, USA
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Jacob L. Yates
3Department of Biology and Program in Neuroscience and Cognitive Science, University of Maryland, USA
4Herbert Wertheim School of Optometry and Vision Science, University of California, USA
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Jude F. Mitchell
5Department of Brain and Cognitive Sciences and Center for Visual Sciences, University of Rochester, USA
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  • For correspondence: cniell@uoregon.edu jmitchell@bcs.rochester.edu
Cristopher M. Niell
1Institute of Neuroscience and Department of Biology, University of Oregon, USA
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  • For correspondence: cniell@uoregon.edu jmitchell@bcs.rochester.edu
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Abstract

Animals move their head and eyes as they explore and sample the visual scene. Previous studies have demonstrated neural correlates of head and eye movements in rodent primary visual cortex (V1), but the sources and computational roles of these signals are unclear. We addressed this by combining measurement of head and eye movements with high density neural recordings in freely moving mice. V1 neurons responded primarily to gaze shifts, where head movements are accompanied by saccadic eye movements, but not to head movements where compensatory eye movements stabilize gaze. A variety of activity patterns immediately followed gaze shifts, including units with positive, biphasic, or negative responses, and together these responses formed a temporal sequence following the gaze shift. These responses were greatly diminished in the dark for the vast majority of units, replaced by a uniform suppression of activity, and were similar to those evoked by sequentially flashed stimuli in head-fixed conditions, suggesting that gaze shift transients represent the temporal response to the rapid onset of new visual input. Notably, neurons responded in a sequence that matches their spatial frequency preference, from low to high spatial frequency tuning, consistent with coarse-to-fine processing of the visual scene following each gaze shift. Recordings in foveal V1 of freely gazing head-fixed marmosets revealed a similar sequence of temporal response following a saccade, as well as the progression of spatial frequency tuning. Together, our results demonstrate that active vision in both mice and marmosets consists of a dynamic temporal sequence of neural activity associated with visual sampling.

Highlights

  • During free movement, neurons in mouse V1 respond to head movements that are accompanied by a gaze-shifting saccadic eye movement, but not a compensatory eye movement.

  • Neurons respond to gaze shifts with diverse temporal dynamics that form a sequence across the population, from early positive responses to biphasic and negative responses.

  • In darkness, most neurons show a uniform suppression following a gaze shift.

  • Temporal dynamics of responses correspond to a neuron’s temporal and spatial frequency preferences, consistent with a coarse-to-fine processing sequence.

  • A similar temporal sequence following saccades is observed in foveal V1 of freely gazing head-fixed marmosets, demonstrating shared aspects of active visual processing across species.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted August 25, 2022.
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A dynamic sequence of visual processing initiated by gaze shifts
Philip R. L. Parker, Dylan M. Martins, Emmalyn S. P. Leonard, Nathan M. Casey, Shelby L. Sharp, Elliott T. T. Abe, Matthew C. Smear, Jacob L. Yates, Jude F. Mitchell, Cristopher M. Niell
bioRxiv 2022.08.23.504847; doi: https://doi.org/10.1101/2022.08.23.504847
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A dynamic sequence of visual processing initiated by gaze shifts
Philip R. L. Parker, Dylan M. Martins, Emmalyn S. P. Leonard, Nathan M. Casey, Shelby L. Sharp, Elliott T. T. Abe, Matthew C. Smear, Jacob L. Yates, Jude F. Mitchell, Cristopher M. Niell
bioRxiv 2022.08.23.504847; doi: https://doi.org/10.1101/2022.08.23.504847

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