Early Sensory Deprivation Leads to Differential Inhibitory Changes in the Striatum During Learning

The corticostriatal circuit has been identified as a vital pathway for associative learning. However, how learning is implemented when the sensory striatum is permanently impaired remains unclear. Using chemogenetic techniques to suppress layer five auditory cortex (AC) input to the auditory striatu...

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Main Authors: Nihaad Paraouty, Todd M. Mowery
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-05-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fncir.2021.670858/full
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author Nihaad Paraouty
Todd M. Mowery
Todd M. Mowery
author_facet Nihaad Paraouty
Todd M. Mowery
Todd M. Mowery
author_sort Nihaad Paraouty
collection DOAJ
description The corticostriatal circuit has been identified as a vital pathway for associative learning. However, how learning is implemented when the sensory striatum is permanently impaired remains unclear. Using chemogenetic techniques to suppress layer five auditory cortex (AC) input to the auditory striatum, learning of a sound discrimination task was significantly impacted in freely moving Mongolian gerbils, in particular when this suppression occurs early on during learning. Whole-cell recordings sampled throughout learning revealed a transient reduction in postsynaptic (GABAA) inhibition in both striatal D1 and D2 cells in normal-hearing gerbils during task acquisition. In contrast, when the baseline striatal inhibitory strengths and firing rates were permanently reduced by a transient period of developmental sensory deprivation, learning was accompanied by augmented inhibition and increased firing rates. Direct manipulation of striatal inhibition in vivo and in vitro revealed a key role of the transient inhibitory changes in task acquisition. Together, these results reveal a flexible corticostriatal inhibitory synaptic plasticity mechanism that accompanies associative auditory learning.
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spelling doaj.art-5a7fa3a5633f49cc80fc8ccec712c2fd2022-12-21T22:30:46ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102021-05-011510.3389/fncir.2021.670858670858Early Sensory Deprivation Leads to Differential Inhibitory Changes in the Striatum During LearningNihaad Paraouty0Todd M. Mowery1Todd M. Mowery2Center for Neural Science, New York University, New York, NY, United StatesDepartment of Otolaryngology, Head and Neck Surgery, Rutgers Robert Wood Johnson Medical School, New Brunswick, NJ, United StatesRutgers Brain Health Institute, Rutgers University, New Brunswick, NJ, United StatesThe corticostriatal circuit has been identified as a vital pathway for associative learning. However, how learning is implemented when the sensory striatum is permanently impaired remains unclear. Using chemogenetic techniques to suppress layer five auditory cortex (AC) input to the auditory striatum, learning of a sound discrimination task was significantly impacted in freely moving Mongolian gerbils, in particular when this suppression occurs early on during learning. Whole-cell recordings sampled throughout learning revealed a transient reduction in postsynaptic (GABAA) inhibition in both striatal D1 and D2 cells in normal-hearing gerbils during task acquisition. In contrast, when the baseline striatal inhibitory strengths and firing rates were permanently reduced by a transient period of developmental sensory deprivation, learning was accompanied by augmented inhibition and increased firing rates. Direct manipulation of striatal inhibition in vivo and in vitro revealed a key role of the transient inhibitory changes in task acquisition. Together, these results reveal a flexible corticostriatal inhibitory synaptic plasticity mechanism that accompanies associative auditory learning.https://www.frontiersin.org/articles/10.3389/fncir.2021.670858/fullcorticostriatal pathwayassociative learningauditory discriminationmedium spiny neuronlayer 5 neuronssynaptic inhibition
spellingShingle Nihaad Paraouty
Todd M. Mowery
Todd M. Mowery
Early Sensory Deprivation Leads to Differential Inhibitory Changes in the Striatum During Learning
Frontiers in Neural Circuits
corticostriatal pathway
associative learning
auditory discrimination
medium spiny neuron
layer 5 neurons
synaptic inhibition
title Early Sensory Deprivation Leads to Differential Inhibitory Changes in the Striatum During Learning
title_full Early Sensory Deprivation Leads to Differential Inhibitory Changes in the Striatum During Learning
title_fullStr Early Sensory Deprivation Leads to Differential Inhibitory Changes in the Striatum During Learning
title_full_unstemmed Early Sensory Deprivation Leads to Differential Inhibitory Changes in the Striatum During Learning
title_short Early Sensory Deprivation Leads to Differential Inhibitory Changes in the Striatum During Learning
title_sort early sensory deprivation leads to differential inhibitory changes in the striatum during learning
topic corticostriatal pathway
associative learning
auditory discrimination
medium spiny neuron
layer 5 neurons
synaptic inhibition
url https://www.frontiersin.org/articles/10.3389/fncir.2021.670858/full
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