How many neurons are sufficient for perception of cortical activity?

Many theories of brain function propose that activity in sparse subsets of neurons underlies perception and action. To place a lower bound on the amount of neural activity that can be perceived, we used an all-optical approach to drive behaviour with targeted two-photon optogenetic activation of sma...

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Main Authors: Henry WP Dalgleish, Lloyd E Russell, Adam M Packer, Arnd Roth, Oliver M Gauld, Francesca Greenstreet, Emmett J Thompson, Michael Häusser
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/58889
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author Henry WP Dalgleish
Lloyd E Russell
Adam M Packer
Arnd Roth
Oliver M Gauld
Francesca Greenstreet
Emmett J Thompson
Michael Häusser
author_facet Henry WP Dalgleish
Lloyd E Russell
Adam M Packer
Arnd Roth
Oliver M Gauld
Francesca Greenstreet
Emmett J Thompson
Michael Häusser
author_sort Henry WP Dalgleish
collection DOAJ
description Many theories of brain function propose that activity in sparse subsets of neurons underlies perception and action. To place a lower bound on the amount of neural activity that can be perceived, we used an all-optical approach to drive behaviour with targeted two-photon optogenetic activation of small ensembles of L2/3 pyramidal neurons in mouse barrel cortex while simultaneously recording local network activity with two-photon calcium imaging. By precisely titrating the number of neurons stimulated, we demonstrate that the lower bound for perception of cortical activity is ~14 pyramidal neurons. We find a steep sigmoidal relationship between the number of activated neurons and behaviour, saturating at only ~37 neurons, and show this relationship can shift with learning. Furthermore, activation of ensembles is balanced by inhibition of neighbouring neurons. This surprising perceptual sensitivity in the face of potent network suppression supports the sparse coding hypothesis, and suggests that cortical perception balances a trade-off between minimizing the impact of noise while efficiently detecting relevant signals.
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spelling doaj.art-568dd0dcd67b495aa79310429cc1bc592022-12-22T03:51:18ZengeLife Sciences Publications LtdeLife2050-084X2020-10-01910.7554/eLife.58889How many neurons are sufficient for perception of cortical activity?Henry WP Dalgleish0https://orcid.org/0000-0002-2390-6361Lloyd E Russell1https://orcid.org/0000-0001-6332-756XAdam M Packer2https://orcid.org/0000-0001-5884-794XArnd Roth3https://orcid.org/0000-0003-0325-4287Oliver M Gauld4Francesca Greenstreet5Emmett J Thompson6Michael Häusser7https://orcid.org/0000-0002-2673-8957Wolfson Institute for Biomedical Research, University College London, London, United KingdomWolfson Institute for Biomedical Research, University College London, London, United KingdomWolfson Institute for Biomedical Research, University College London, London, United KingdomWolfson Institute for Biomedical Research, University College London, London, United KingdomWolfson Institute for Biomedical Research, University College London, London, United KingdomWolfson Institute for Biomedical Research, University College London, London, United KingdomWolfson Institute for Biomedical Research, University College London, London, United KingdomWolfson Institute for Biomedical Research, University College London, London, United KingdomMany theories of brain function propose that activity in sparse subsets of neurons underlies perception and action. To place a lower bound on the amount of neural activity that can be perceived, we used an all-optical approach to drive behaviour with targeted two-photon optogenetic activation of small ensembles of L2/3 pyramidal neurons in mouse barrel cortex while simultaneously recording local network activity with two-photon calcium imaging. By precisely titrating the number of neurons stimulated, we demonstrate that the lower bound for perception of cortical activity is ~14 pyramidal neurons. We find a steep sigmoidal relationship between the number of activated neurons and behaviour, saturating at only ~37 neurons, and show this relationship can shift with learning. Furthermore, activation of ensembles is balanced by inhibition of neighbouring neurons. This surprising perceptual sensitivity in the face of potent network suppression supports the sparse coding hypothesis, and suggests that cortical perception balances a trade-off between minimizing the impact of noise while efficiently detecting relevant signals.https://elifesciences.org/articles/58889cortexneural codingoptogenetics2-photon imagingperceptionbehaviour
spellingShingle Henry WP Dalgleish
Lloyd E Russell
Adam M Packer
Arnd Roth
Oliver M Gauld
Francesca Greenstreet
Emmett J Thompson
Michael Häusser
How many neurons are sufficient for perception of cortical activity?
eLife
cortex
neural coding
optogenetics
2-photon imaging
perception
behaviour
title How many neurons are sufficient for perception of cortical activity?
title_full How many neurons are sufficient for perception of cortical activity?
title_fullStr How many neurons are sufficient for perception of cortical activity?
title_full_unstemmed How many neurons are sufficient for perception of cortical activity?
title_short How many neurons are sufficient for perception of cortical activity?
title_sort how many neurons are sufficient for perception of cortical activity
topic cortex
neural coding
optogenetics
2-photon imaging
perception
behaviour
url https://elifesciences.org/articles/58889
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