Associative learning changes the organization of functional excitatory circuits targeting the supragranular layers of mouse barrel cortex

In primary sensory cortices, neuronal circuits change throughout life as a function of learning. During associative learning a neutral sensory stimulus acquires the emotional valence of an aversive event or a reward after repetitive contingent pairing. One important consequence is the enlargement of...

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Main Authors: Céline eRosselet, Maxime eFieschi, Sandrine eHugues, Ingrid eBureau
Format: Article
Language:English
Published: Frontiers Media S.A. 2011-01-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fncir.2010.00126/full
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spelling doaj-4d7e62c4070f406aaad9331bf93d740c2020-11-25T00:02:01ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102011-01-01410.3389/fncir.2010.001268482Associative learning changes the organization of functional excitatory circuits targeting the supragranular layers of mouse barrel cortexCéline eRosselet0Céline eRosselet1Maxime eFieschi2Maxime eFieschi3Sandrine eHugues4Sandrine eHugues5Ingrid eBureau6Ingrid eBureau7INSERMUniversité de la MéditerranéeINSERMUniversité de la MéditerranéeINSERMUniversité de la MéditerranéeINSERMUniversité de la MéditerranéeIn primary sensory cortices, neuronal circuits change throughout life as a function of learning. During associative learning a neutral sensory stimulus acquires the emotional valence of an aversive event or a reward after repetitive contingent pairing. One important consequence is the enlargement of the representational area of the conditioned stimulus in the cortical map of its sensory modality. The details of this phenomenon at the circuit level are still largely unknown.Here, mice were trained in a differential conditioning paradigm where the deflections of one whisker row were paired with tail shocks and the deflections of two others were not. Changes occurring in excitatory circuits of barrel cortex were then examined in brain slices with laser scanning photostimulation mapping. We found that learning affected the projections targeting the supragranular layers in the columns of unpaired whiskers: Pyramidal cells located in layer (L) 3 received enhanced inputs from L5A cells located in their home column and new inputs from L2/3 and L4 cells located in the neighboring column of the paired whisker. In contrast, the excitatory projections impinging onto L2/3 cells in the column of the paired whisker were not altered. Together, these data reveal that associative learning alters the canonical columnar organization of functional ascending L4 projections and strengthens transcolumnar excitatory projections in barrel cortex. These phenomena could participate to the transformation of the whisker somatotopic map induced by associative learning.http://journal.frontiersin.org/Journal/10.3389/fncir.2010.00126/fullFear conditioningCortical CircuitsSynaptic connectivityGlutamate Uncaginglayer 2/3
collection DOAJ
language English
format Article
sources DOAJ
author Céline eRosselet
Céline eRosselet
Maxime eFieschi
Maxime eFieschi
Sandrine eHugues
Sandrine eHugues
Ingrid eBureau
Ingrid eBureau
spellingShingle Céline eRosselet
Céline eRosselet
Maxime eFieschi
Maxime eFieschi
Sandrine eHugues
Sandrine eHugues
Ingrid eBureau
Ingrid eBureau
Associative learning changes the organization of functional excitatory circuits targeting the supragranular layers of mouse barrel cortex
Frontiers in Neural Circuits
Fear conditioning
Cortical Circuits
Synaptic connectivity
Glutamate Uncaging
layer 2/3
author_facet Céline eRosselet
Céline eRosselet
Maxime eFieschi
Maxime eFieschi
Sandrine eHugues
Sandrine eHugues
Ingrid eBureau
Ingrid eBureau
author_sort Céline eRosselet
title Associative learning changes the organization of functional excitatory circuits targeting the supragranular layers of mouse barrel cortex
title_short Associative learning changes the organization of functional excitatory circuits targeting the supragranular layers of mouse barrel cortex
title_full Associative learning changes the organization of functional excitatory circuits targeting the supragranular layers of mouse barrel cortex
title_fullStr Associative learning changes the organization of functional excitatory circuits targeting the supragranular layers of mouse barrel cortex
title_full_unstemmed Associative learning changes the organization of functional excitatory circuits targeting the supragranular layers of mouse barrel cortex
title_sort associative learning changes the organization of functional excitatory circuits targeting the supragranular layers of mouse barrel cortex
publisher Frontiers Media S.A.
series Frontiers in Neural Circuits
issn 1662-5110
publishDate 2011-01-01
description In primary sensory cortices, neuronal circuits change throughout life as a function of learning. During associative learning a neutral sensory stimulus acquires the emotional valence of an aversive event or a reward after repetitive contingent pairing. One important consequence is the enlargement of the representational area of the conditioned stimulus in the cortical map of its sensory modality. The details of this phenomenon at the circuit level are still largely unknown.Here, mice were trained in a differential conditioning paradigm where the deflections of one whisker row were paired with tail shocks and the deflections of two others were not. Changes occurring in excitatory circuits of barrel cortex were then examined in brain slices with laser scanning photostimulation mapping. We found that learning affected the projections targeting the supragranular layers in the columns of unpaired whiskers: Pyramidal cells located in layer (L) 3 received enhanced inputs from L5A cells located in their home column and new inputs from L2/3 and L4 cells located in the neighboring column of the paired whisker. In contrast, the excitatory projections impinging onto L2/3 cells in the column of the paired whisker were not altered. Together, these data reveal that associative learning alters the canonical columnar organization of functional ascending L4 projections and strengthens transcolumnar excitatory projections in barrel cortex. These phenomena could participate to the transformation of the whisker somatotopic map induced by associative learning.
topic Fear conditioning
Cortical Circuits
Synaptic connectivity
Glutamate Uncaging
layer 2/3
url http://journal.frontiersin.org/Journal/10.3389/fncir.2010.00126/full
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