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Synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus

Corticofugal projections to evolutionarily ancient, subcortical structures are ubiquitous across mammalian sensory systems. These ‘descending’ pathways enable the neocortex to control ascending sensory representations in a predictive or feedback manner, but the underlying cellular mechanisms are poo...

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Autores principales: Oberle, Hannah M, Ford, Alexander N, Dileepkumar, Deepak, Czarny, Jordyn, Apostolides, Pierre F
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8735864/
https://www.ncbi.nlm.nih.gov/pubmed/34989674
http://dx.doi.org/10.7554/eLife.72730
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author Oberle, Hannah M
Ford, Alexander N
Dileepkumar, Deepak
Czarny, Jordyn
Apostolides, Pierre F
author_facet Oberle, Hannah M
Ford, Alexander N
Dileepkumar, Deepak
Czarny, Jordyn
Apostolides, Pierre F
author_sort Oberle, Hannah M
collection PubMed
description Corticofugal projections to evolutionarily ancient, subcortical structures are ubiquitous across mammalian sensory systems. These ‘descending’ pathways enable the neocortex to control ascending sensory representations in a predictive or feedback manner, but the underlying cellular mechanisms are poorly understood. Here, we combine optogenetic approaches with in vivo and in vitro patch-clamp electrophysiology to study the projection from mouse auditory cortex to the inferior colliculus (IC), a major descending auditory pathway that controls IC neuron feature selectivity, plasticity, and auditory perceptual learning. Although individual auditory cortico-collicular synapses were generally weak, IC neurons often integrated inputs from multiple corticofugal axons that generated reliable, tonic depolarizations even during prolonged presynaptic activity. Latency measurements in vivo showed that descending signals reach the IC within 30 ms of sound onset, which in IC neurons corresponded to the peak of synaptic depolarizations evoked by short sounds. Activating ascending and descending pathways at latencies expected in vivo caused a NMDA receptor-dependent, supralinear excitatory postsynaptic potential summation, indicating that descending signals can nonlinearly amplify IC neurons’ moment-to-moment acoustic responses. Our results shed light upon the synaptic bases of descending sensory control and imply that heterosynaptic cooperativity contributes to the auditory cortico-collicular pathway’s role in plasticity and perceptual learning.
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spelling pubmed-87358642022-01-07 Synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus Oberle, Hannah M Ford, Alexander N Dileepkumar, Deepak Czarny, Jordyn Apostolides, Pierre F eLife Neuroscience Corticofugal projections to evolutionarily ancient, subcortical structures are ubiquitous across mammalian sensory systems. These ‘descending’ pathways enable the neocortex to control ascending sensory representations in a predictive or feedback manner, but the underlying cellular mechanisms are poorly understood. Here, we combine optogenetic approaches with in vivo and in vitro patch-clamp electrophysiology to study the projection from mouse auditory cortex to the inferior colliculus (IC), a major descending auditory pathway that controls IC neuron feature selectivity, plasticity, and auditory perceptual learning. Although individual auditory cortico-collicular synapses were generally weak, IC neurons often integrated inputs from multiple corticofugal axons that generated reliable, tonic depolarizations even during prolonged presynaptic activity. Latency measurements in vivo showed that descending signals reach the IC within 30 ms of sound onset, which in IC neurons corresponded to the peak of synaptic depolarizations evoked by short sounds. Activating ascending and descending pathways at latencies expected in vivo caused a NMDA receptor-dependent, supralinear excitatory postsynaptic potential summation, indicating that descending signals can nonlinearly amplify IC neurons’ moment-to-moment acoustic responses. Our results shed light upon the synaptic bases of descending sensory control and imply that heterosynaptic cooperativity contributes to the auditory cortico-collicular pathway’s role in plasticity and perceptual learning. eLife Sciences Publications, Ltd 2022-01-06 /pmc/articles/PMC8735864/ /pubmed/34989674 http://dx.doi.org/10.7554/eLife.72730 Text en © 2021, Oberle et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Oberle, Hannah M
Ford, Alexander N
Dileepkumar, Deepak
Czarny, Jordyn
Apostolides, Pierre F
Synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus
title Synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus
title_full Synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus
title_fullStr Synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus
title_full_unstemmed Synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus
title_short Synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus
title_sort synaptic mechanisms of top-down control in the non-lemniscal inferior colliculus
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8735864/
https://www.ncbi.nlm.nih.gov/pubmed/34989674
http://dx.doi.org/10.7554/eLife.72730
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