Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex

Daily exposure of awake mice to a phase-reversing visual grating stimulus leads to enhancement of the visual-evoked potential (VEP) in layer 4 of the primary visual cortex (V1). This stimulus-selective response potentiation (SRP) resembles and shares mechanistic requirements with canonical long-term...

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Main Authors: Kim, Taekeun, Harnett, Mark T., Bear, Mark F.
Other Authors: Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Format: Article
Language:English
Published: Frontiers Media SA 2020
Subjects:
Online Access:https://hdl.handle.net/1721.1/124487
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author Kim, Taekeun
Harnett, Mark T.
Bear, Mark F.
author2 Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
author_facet Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Kim, Taekeun
Harnett, Mark T.
Bear, Mark F.
author_sort Kim, Taekeun
collection MIT
description Daily exposure of awake mice to a phase-reversing visual grating stimulus leads to enhancement of the visual-evoked potential (VEP) in layer 4 of the primary visual cortex (V1). This stimulus-selective response potentiation (SRP) resembles and shares mechanistic requirements with canonical long-term synaptic potentiation (LTP). However, it remains to be determined how this augmentation of a population response translates into altered neuronal activity of individual V1 neurons. To address this question, we performed longitudinal calcium imaging of layer 4 excitatory neurons in V1 and tracked changes associated with the induction and expression of SRP. We found no evidence for a net change in the fraction of visually responsive neurons as the stimulus became familiar. However, endoscopic calcium imaging of layer 4 principal neurons revealed that somatic calcium transients in response to phase-reversals of the familiar visual stimulus are reduced and undergo strong within-session adaptation. Conversely, neuropil calcium responses and VEPs are enhanced during familiar stimulus viewing, and the VEPs show reduced within-session adaptation. Consistent with the exquisite selectivity of SRP, the plasticity of cellular responses to phase-reversing gratings did not translate into altered orientation selectivity to drifting gratings. Our findings suggest a model in which augmentation of fast, short-latency synaptic (dendritic) responses, manifested as enhanced layer 4 VEPs, recruits inhibition to suppress cellular activity. Reduced cellular activity to the familiar stimulus may account for the behavioral correlate of SRP, orientation-selective long-term habituation.
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spelling mit-1721.1/1244872022-10-03T09:15:35Z Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex Kim, Taekeun Harnett, Mark T. Bear, Mark F. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Cellular and Molecular Neuroscience Daily exposure of awake mice to a phase-reversing visual grating stimulus leads to enhancement of the visual-evoked potential (VEP) in layer 4 of the primary visual cortex (V1). This stimulus-selective response potentiation (SRP) resembles and shares mechanistic requirements with canonical long-term synaptic potentiation (LTP). However, it remains to be determined how this augmentation of a population response translates into altered neuronal activity of individual V1 neurons. To address this question, we performed longitudinal calcium imaging of layer 4 excitatory neurons in V1 and tracked changes associated with the induction and expression of SRP. We found no evidence for a net change in the fraction of visually responsive neurons as the stimulus became familiar. However, endoscopic calcium imaging of layer 4 principal neurons revealed that somatic calcium transients in response to phase-reversals of the familiar visual stimulus are reduced and undergo strong within-session adaptation. Conversely, neuropil calcium responses and VEPs are enhanced during familiar stimulus viewing, and the VEPs show reduced within-session adaptation. Consistent with the exquisite selectivity of SRP, the plasticity of cellular responses to phase-reversing gratings did not translate into altered orientation selectivity to drifting gratings. Our findings suggest a model in which augmentation of fast, short-latency synaptic (dendritic) responses, manifested as enhanced layer 4 VEPs, recruits inhibition to suppress cellular activity. Reduced cellular activity to the familiar stimulus may account for the behavioral correlate of SRP, orientation-selective long-term habituation. National Institutes of Health (U.S.) (R01EY023037) 2020-04-03T12:18:15Z 2020-04-03T12:18:15Z 2020-01-14 2020-02-11T17:44:15Z Article http://purl.org/eprint/type/JournalArticle 1662-5102 https://hdl.handle.net/1721.1/124487 Kim, Taekeun et al. "Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex." Frontiers in Cellular Neuroscience 13 (2020): article 555 © 2020 The Author(s) en 10.3389/fncel.2019.00555 Frontiers in Cellular Neuroscience Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/ application/pdf Frontiers Media SA Frontiers
spellingShingle Cellular and Molecular Neuroscience
Kim, Taekeun
Harnett, Mark T.
Bear, Mark F.
Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex
title Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex
title_full Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex
title_fullStr Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex
title_full_unstemmed Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex
title_short Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex
title_sort opposing somatic and dendritic expression of stimulus selective response plasticity in mouse primary visual cortex
topic Cellular and Molecular Neuroscience
url https://hdl.handle.net/1721.1/124487
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