Synthesis of a comprehensive population code for contextual features in the awake sensory cortex
- UC Berkeley, United States
- Purdue University, United States
- The Hebrew University of Jerusalem, Israel
- University of California, Berkeley, United States
Abstract
How cortical circuits build representations of complex objects is poorly understood. Individual neurons must integrate broadly over space, yet simultaneously obtain sharp tuning to specific global stimulus features. Groups of neurons identifying different global features must then assemble into a population that forms a comprehensive code for these global stimulus properties. Although the logic for how single neurons summate over their spatial inputs has been well-explored in anesthetized animals, how large groups of neurons compose a flexible population code of higher order features in awake animals is not known. To address this question, we probed the integration and population coding of higher order stimuli in the somatosensory and visual cortices of awake mice using two-photon calcium imaging across cortical layers. We developed a novel tactile stimulator that allowed the precise measurement of spatial summation even in actively whisking mice. Using this system, we found a sparse but comprehensive population code for higher order tactile features that depends on a heterogeneous and neuron-specific logic of spatial summation beyond the receptive field. Different somatosensory cortical neurons summed specific combinations of sensory inputs supra-linearly, but integrated other inputs sub-linearly, leading to selective responses to higher order features. Visual cortical populations employed a nearly identical scheme to generate a comprehensive population code for contextual stimuli. These results suggest that a heterogeneous logic of input-specific supra-linear summation may represent a widespread cortical mechanism for the synthesis of sparse higher order feature codes in neural populations. This may explain how the brain exploits the thalamocortical expansion of dimensionality to encode arbitrary complex features of sensory stimuli.
Data availability
All source data and analysis software is uploaded to Dryad.
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Data supporting "Synthesis of higher order feature codes through stimulus-specific supra-linear summation"Dryad Digital Repository, doi:10.6078/D1370M.
Article and author information
Author details
Funding
NIH Office of the Director (DP2NS087725)
- Hillel Adesnik
National Eye Institute (R01EY023756)
- Hillel Adesnik
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Brice Bathellier, CNRS, France
Ethics
Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (ACUC) protocols AUP-2014-10-6832-2 of the University of California, Berkeley. All surgery was performed under isoflurane anesthesia, and every effort was made to minimize suffering.
Version history
- Received: September 1, 2020
- Accepted: October 25, 2021
- Accepted Manuscript published: November 1, 2021 (version 1)
- Version of Record published: November 17, 2021 (version 2)
Copyright
© 2021, Lyall et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Synthesis of a comprehensive population code for contextual features in the awake sensory cortex
eLife 10:e62687.
https://doi.org/10.7554/eLife.62687
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