State-dependent pupil dilation rapidly shifts visual feature selectivity

Katrin Franke (), Konstantin F. Willeke, Kayla Ponder, Mario Galdamez, Na Zhou, Taliah Muhammad, Saumil Patel, Emmanouil Froudarakis, Jacob Reimer, Fabian H. Sinz and Andreas S. Tolias
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Katrin Franke: Tübingen University
Konstantin F. Willeke: Tübingen University
Kayla Ponder: Baylor College of Medicine
Mario Galdamez: Baylor College of Medicine
Na Zhou: Baylor College of Medicine
Taliah Muhammad: Baylor College of Medicine
Saumil Patel: Baylor College of Medicine
Emmanouil Froudarakis: Baylor College of Medicine
Jacob Reimer: Baylor College of Medicine
Fabian H. Sinz: Baylor College of Medicine
Andreas S. Tolias: Baylor College of Medicine

Nature, 2022, vol. 610, issue 7930, 128-134

Abstract: 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 dilation1,2 enhance sensory responses, but typically leave the preferred stimuli of neurons unchanged2–9. 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 sky10. 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.

Date: 2022
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DOI: 10.1038/s41586-022-05270-3

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