Coordinated multiplexing of information about separate objects in visual cortex

Sensory receptive fields are large enough that they can contain more than one perceptible stimulus. How, then, can the brain encode information about each of the stimuli that may be present at a given moment? We recently showed that when more than one stimulus is present, single neurons can fluctuat...

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Main Authors: Na Young Jun, Douglas A Ruff, Lily E Kramer, Brittany Bowes, Surya T Tokdar, Marlene R Cohen, Jennifer M Groh
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/76452
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author Na Young Jun
Douglas A Ruff
Lily E Kramer
Brittany Bowes
Surya T Tokdar
Marlene R Cohen
Jennifer M Groh
author_facet Na Young Jun
Douglas A Ruff
Lily E Kramer
Brittany Bowes
Surya T Tokdar
Marlene R Cohen
Jennifer M Groh
author_sort Na Young Jun
collection DOAJ
description Sensory receptive fields are large enough that they can contain more than one perceptible stimulus. How, then, can the brain encode information about each of the stimuli that may be present at a given moment? We recently showed that when more than one stimulus is present, single neurons can fluctuate between coding one vs. the other(s) across some time period, suggesting a form of neural multiplexing of different stimuli (Caruso et al., 2018). Here, we investigate (a) whether such coding fluctuations occur in early visual cortical areas; (b) how coding fluctuations are coordinated across the neural population; and (c) how coordinated coding fluctuations depend on the parsing of stimuli into separate vs. fused objects. We found coding fluctuations do occur in macaque V1 but only when the two stimuli form separate objects. Such separate objects evoked a novel pattern of V1 spike count (‘noise’) correlations involving distinct distributions of positive and negative values. This bimodal correlation pattern was most pronounced among pairs of neurons showing the strongest evidence for coding fluctuations or multiplexing. Whether a given pair of neurons exhibited positive or negative correlations depended on whether the two neurons both responded better to the same object or had different object preferences. Distinct distributions of spike count correlations based on stimulus preferences were also seen in V4 for separate objects but not when two stimuli fused to form one object. These findings suggest multiple objects evoke different response dynamics than those evoked by single stimuli, lending support to the multiplexing hypothesis and suggesting a means by which information about multiple objects can be preserved despite the apparent coarseness of sensory coding.
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spelling doaj.art-cf89de33b5f542f68b80f974369890542022-12-22T04:16:51ZengeLife Sciences Publications LtdeLife2050-084X2022-11-011110.7554/eLife.76452Coordinated multiplexing of information about separate objects in visual cortexNa Young Jun0https://orcid.org/0000-0002-8841-3947Douglas A Ruff1Lily E Kramer2Brittany Bowes3Surya T Tokdar4Marlene R Cohen5Jennifer M Groh6https://orcid.org/0000-0002-6435-3935Department of Neurobiology, Duke University, Durham, United States; Center for Cognitive Neuroscience, Duke University, Durham, United States; Duke Institute for Brain Sciences, Durham, United StatesDepartment of Neuroscience, University of Pittsburgh, Pittsburgh, United States; Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, United StatesDepartment of Neuroscience, University of Pittsburgh, Pittsburgh, United States; Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, United StatesDepartment of Neuroscience, University of Pittsburgh, Pittsburgh, United States; Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, United StatesDepartment of Statistical Science, Duke University, Durham, United StatesDepartment of Neuroscience, University of Pittsburgh, Pittsburgh, United States; Center for the Neural Basis of Cognition, University of Pittsburgh, Pittsburgh, United StatesDepartment of Neurobiology, Duke University, Durham, United States; Center for Cognitive Neuroscience, Duke University, Durham, United States; Duke Institute for Brain Sciences, Durham, United States; Department of Psychology and Neuroscience, Duke University, Durham, United States; Department of Biomedical Engineering, Duke University, Durham, United States; Department of Computer Science, Duke University, Durham, United StatesSensory receptive fields are large enough that they can contain more than one perceptible stimulus. How, then, can the brain encode information about each of the stimuli that may be present at a given moment? We recently showed that when more than one stimulus is present, single neurons can fluctuate between coding one vs. the other(s) across some time period, suggesting a form of neural multiplexing of different stimuli (Caruso et al., 2018). Here, we investigate (a) whether such coding fluctuations occur in early visual cortical areas; (b) how coding fluctuations are coordinated across the neural population; and (c) how coordinated coding fluctuations depend on the parsing of stimuli into separate vs. fused objects. We found coding fluctuations do occur in macaque V1 but only when the two stimuli form separate objects. Such separate objects evoked a novel pattern of V1 spike count (‘noise’) correlations involving distinct distributions of positive and negative values. This bimodal correlation pattern was most pronounced among pairs of neurons showing the strongest evidence for coding fluctuations or multiplexing. Whether a given pair of neurons exhibited positive or negative correlations depended on whether the two neurons both responded better to the same object or had different object preferences. Distinct distributions of spike count correlations based on stimulus preferences were also seen in V4 for separate objects but not when two stimuli fused to form one object. These findings suggest multiple objects evoke different response dynamics than those evoked by single stimuli, lending support to the multiplexing hypothesis and suggesting a means by which information about multiple objects can be preserved despite the apparent coarseness of sensory coding.https://elifesciences.org/articles/76452noise correlationsvariabilitymultiplexingpopulation codingobject vision
spellingShingle Na Young Jun
Douglas A Ruff
Lily E Kramer
Brittany Bowes
Surya T Tokdar
Marlene R Cohen
Jennifer M Groh
Coordinated multiplexing of information about separate objects in visual cortex
eLife
noise correlations
variability
multiplexing
population coding
object vision
title Coordinated multiplexing of information about separate objects in visual cortex
title_full Coordinated multiplexing of information about separate objects in visual cortex
title_fullStr Coordinated multiplexing of information about separate objects in visual cortex
title_full_unstemmed Coordinated multiplexing of information about separate objects in visual cortex
title_short Coordinated multiplexing of information about separate objects in visual cortex
title_sort coordinated multiplexing of information about separate objects in visual cortex
topic noise correlations
variability
multiplexing
population coding
object vision
url https://elifesciences.org/articles/76452
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