A latent pool of neurons silenced by sensory-evoked inhibition can be recruited to enhance perception

Oliver M Gauld; Adam M Packer; Lloyd E Russell; Henry W P Dalgleish; Maya Iuga; Francisco Sacadura; Arnd Roth; Beverley A Clark; Michael Häusser

doi:10.1016/j.neuron.2024.04.015

A latent pool of neurons silenced by sensory-evoked inhibition can be recruited to enhance perception

Neuron. 2024 May 8:S0896-6273(24)00276-9. doi: 10.1016/j.neuron.2024.04.015. Online ahead of print.

Authors

Oliver M Gauld¹, Adam M Packer², Lloyd E Russell³, Henry W P Dalgleish³, Maya Iuga³, Francisco Sacadura³, Arnd Roth³, Beverley A Clark³, Michael Häusser⁴

Affiliations

¹ Wolfson Institute for Biomedical Research, University College London, London WC1E 6BT, UK; Sainsbury Wellcome Centre, University College London, London W1T 4JG, UK. Electronic address: o.gauld@ucl.ac.uk.
² Wolfson Institute for Biomedical Research, University College London, London WC1E 6BT, UK; Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, UK.
³ Wolfson Institute for Biomedical Research, University College London, London WC1E 6BT, UK.
⁴ Wolfson Institute for Biomedical Research, University College London, London WC1E 6BT, UK. Electronic address: m.hausser@ucl.ac.uk.

PMID: 38729150
DOI: 10.1016/j.neuron.2024.04.015

Abstract

To investigate which activity patterns in sensory cortex are relevant for perceptual decision-making, we combined two-photon calcium imaging and targeted two-photon optogenetics to interrogate barrel cortex activity during perceptual discrimination. We trained mice to discriminate bilateral whisker deflections and report decisions by licking left or right. Two-photon calcium imaging revealed sparse coding of contralateral and ipsilateral whisker input in layer 2/3, with most neurons remaining silent during the task. Activating pyramidal neurons using two-photon holographic photostimulation evoked a perceptual bias that scaled with the number of neurons photostimulated. This effect was dominated by optogenetic activation of non-coding neurons, which did not show sensory or motor-related activity during task performance. Photostimulation also revealed potent recruitment of cortical inhibition during sensory processing, which strongly and preferentially suppressed non-coding neurons. Our results suggest that a pool of non-coding neurons, selectively suppressed by network inhibition during sensory processing, can be recruited to enhance perception.

Keywords: all-optical interrogation; behavior; cortex; optogenetics; sensory processing; sparse coding; two-photon imaging.