Cited by 85Visual perception and processing mechanismsNeural dynamics and brain functionNeuroscience and Neuropharmacology Research

State-dependent pupil dilation rapidly shifts visual feature selectivity

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Franke, Katrin, Willeke, Konstantin F., Ponder, Kayla, Galdamez, Mario, Zhou, Na, Muhammad, Taliah, Patel, Saumil, Froudarakis, Emmanouil +3 more·2022·Nature

Abstract

To increase computational flexibility, the processing of sensory inputs changes with behavioural context. In the visual system, active behavioural states characterized by motor activity and pupil dilation 1,2 enhance sensory responses, but typically leave the preferred stimuli of neurons unchanged 2-9. Here we find that behavioural state also modulates stimulus selectivity in the mouse visual cortex in the context of coloured natural scenes. Using population imaging in behaving mice, pharmacology and deep neural network modelling, we identified a rapid shift in colour selectivity towards ultraviolet stimuli during an active behavioural state. This was exclusively caused by state-dependent pupil dilation, which resulted in a dynamic switch from rod to cone photoreceptors, thereby extending their role beyond night and day vision. The change in tuning facilitated the decoding of ethological stimuli, such as aerial predators against the twilight sky 10. For decades, studies in neuroscience and cognitive science have used pupil dilation as an indirect measure of brain state. Our data suggest that, in addition, state-dependent pupil dilation itself tunes visual representations to behavioural demands by differentially recruiting rods and cones on fast timescales.

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  • Head-restrained preparations have shown that behavioral state fluctuations have a strong impact on neuronal gain and coding properties in primary sensory areas and modulate neuronal firing within brain-wide neuronal networks.

    “By employing head-restrained preparations, a growing body of work has demonstrated that behavioral state fluctuations have a strong impact on neuronal gain and coding properties in primary sensory areas36,43,66–70 and modulate neuronal firing within brain-wide neuronal networks44,71–74.”

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Research works printed but not linked: 3

  1. [13]Busse L. The influence of locomotion on sensory processing and its underlying neuronal circuits. eNeuroforum 24 (1), A41– A51 (2018).
  2. [64]Ioffe S. & Szegedy C. Batch normalization: accelerating deep network training by reducing internal covariate shift, ICML’ 15, 448– 456 (JMLR.org, 2015).
  3. [67]Kingma DP & Ba J. Bengio Y. & LeCun Y. (eds) Adam: A method for stochastic optimization. (eds Bengio Y. & LeCun Y) 3rd International Conference on Learning Representations, ICLR 2015, San Diego, CA, USA, May 7–9, 2015, Conference Track Proceedings (2015).

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Authors
Franke, K., Willeke, K. F., Ponder, K., Galdamez, M., Zhou, N., Muhammad, T., Patel, S., Froudarakis, E., Reimer, J., Sinz, F. H., & Tolias, A. S.
Affiliations
  • Baylor College of Medicine (US)
  • University of Göttingen (DE)
Corresponding author
Franke, Katrin
Venue
Nature
Published
2022-09-28
Volume
610
Issue
7930
Pages
128-134
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W4297497819
Cited by
85
References
69
Citations by year
2026: 28 · 2025: 16 · 2024: 22 · 2023: 17 · 2021: 2
FWCI
7.09
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • GoeScholar The Publication Server of the Georg-August-Universität Göttingen (Georg-August-Universität Göttingen) (submittedVersion, cc-by)
Funders
  • National Science Foundation (1707400)
  • Carl-Zeiss-Stiftung
  • Deutsche Forschungsgemeinschaft (206/4-1, EXC2064, EXC 2064_1, 390727645)
  • National Institutes of Health (T32-EY-002520-37)
  • Intelligence Advanced Research Projects Activity (D16PC00003)
  • Interior Business Center
  • National Eye Institute (T32EY-002520-37, EY-002520-37, R01EY026927, P30EY002520, EY002520)
  • National Institute of General Medical Sciences (R25GM056929)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
pupil dilation, behavioral state, ultraviolet vision, rod photoreceptors, cone photoreceptors, visual cortex, mouse visual system
MeSH terms
Deep Learning, Animals, Color, Darkness, Photic Stimulation, Pupil, Reflex, Pupillary, Time Factors, Ultraviolet Rays, Vision, Ocular, Visual Cortex, Retinal Rod Photoreceptor Cells, Retinal Cone Photoreceptor Cells, Mice

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