Precise sound characteristics drive plasticity in the primary auditory cortex with VNS-sound pairing

IntroductionRepeatedly pairing a tone with vagus nerve stimulation (VNS) alters frequency tuning across the auditory pathway. Pairing VNS with speech sounds selectively enhances the primary auditory cortex response to the paired sounds. It is not yet known how altering the speech sounds paired with...

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Main Authors: Michael S. Borland, Elizabeth P. Buell, Jonathan R. Riley, Alan M. Carroll, Nicole A. Moreno, Pryanka Sharma, Katelyn M. Grasse, John M. Buell, Michael P. Kilgard, Crystal T. Engineer
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2023.1248936/full
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author Michael S. Borland
Michael S. Borland
Elizabeth P. Buell
Elizabeth P. Buell
Jonathan R. Riley
Jonathan R. Riley
Alan M. Carroll
Alan M. Carroll
Nicole A. Moreno
Nicole A. Moreno
Pryanka Sharma
Pryanka Sharma
Katelyn M. Grasse
Katelyn M. Grasse
John M. Buell
John M. Buell
Michael P. Kilgard
Michael P. Kilgard
Crystal T. Engineer
Crystal T. Engineer
author_facet Michael S. Borland
Michael S. Borland
Elizabeth P. Buell
Elizabeth P. Buell
Jonathan R. Riley
Jonathan R. Riley
Alan M. Carroll
Alan M. Carroll
Nicole A. Moreno
Nicole A. Moreno
Pryanka Sharma
Pryanka Sharma
Katelyn M. Grasse
Katelyn M. Grasse
John M. Buell
John M. Buell
Michael P. Kilgard
Michael P. Kilgard
Crystal T. Engineer
Crystal T. Engineer
author_sort Michael S. Borland
collection DOAJ
description IntroductionRepeatedly pairing a tone with vagus nerve stimulation (VNS) alters frequency tuning across the auditory pathway. Pairing VNS with speech sounds selectively enhances the primary auditory cortex response to the paired sounds. It is not yet known how altering the speech sounds paired with VNS alters responses. In this study, we test the hypothesis that the sounds that are presented and paired with VNS will influence the neural plasticity observed following VNS-sound pairing.MethodsTo explore the relationship between acoustic experience and neural plasticity, responses were recorded from primary auditory cortex (A1) after VNS was repeatedly paired with the speech sounds ‘rad’ and ‘lad’ or paired with only the speech sound ‘rad’ while ‘lad’ was an unpaired background sound.ResultsPairing both sounds with VNS increased the response strength and neural discriminability of the paired sounds in the primary auditory cortex. Surprisingly, pairing only ‘rad’ with VNS did not alter A1 responses.DiscussionThese results suggest that the specific acoustic contrasts associated with VNS can powerfully shape neural activity in the auditory pathway. Methods to promote plasticity in the central auditory system represent a new therapeutic avenue to treat auditory processing disorders. Understanding how different sound contrasts and neural activity patterns shape plasticity could have important clinical implications.
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spelling doaj.art-64789a5436734dd3a51b40dd7dcbd7eb2023-09-05T10:10:51ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-09-011710.3389/fnins.2023.12489361248936Precise sound characteristics drive plasticity in the primary auditory cortex with VNS-sound pairingMichael S. Borland0Michael S. Borland1Elizabeth P. Buell2Elizabeth P. Buell3Jonathan R. Riley4Jonathan R. Riley5Alan M. Carroll6Alan M. Carroll7Nicole A. Moreno8Nicole A. Moreno9Pryanka Sharma10Pryanka Sharma11Katelyn M. Grasse12Katelyn M. Grasse13John M. Buell14John M. Buell15Michael P. Kilgard16Michael P. Kilgard17Crystal T. Engineer18Crystal T. Engineer19Department of Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesDepartment of Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesDepartment of Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesDepartment of Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesDepartment of Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesDepartment of Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesErik Jonsson School of Engineering and Computer Science, The University of Texas at Dallas, Richardson, TX, United StatesDepartment of Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesDepartment of Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesDepartment of Neuroscience, School of Behavioral and Brain Sciences, The University of Texas at Dallas, Richardson, TX, United StatesTexas Biomedical Device Center, The University of Texas at Dallas, Richardson, TX, United StatesIntroductionRepeatedly pairing a tone with vagus nerve stimulation (VNS) alters frequency tuning across the auditory pathway. Pairing VNS with speech sounds selectively enhances the primary auditory cortex response to the paired sounds. It is not yet known how altering the speech sounds paired with VNS alters responses. In this study, we test the hypothesis that the sounds that are presented and paired with VNS will influence the neural plasticity observed following VNS-sound pairing.MethodsTo explore the relationship between acoustic experience and neural plasticity, responses were recorded from primary auditory cortex (A1) after VNS was repeatedly paired with the speech sounds ‘rad’ and ‘lad’ or paired with only the speech sound ‘rad’ while ‘lad’ was an unpaired background sound.ResultsPairing both sounds with VNS increased the response strength and neural discriminability of the paired sounds in the primary auditory cortex. Surprisingly, pairing only ‘rad’ with VNS did not alter A1 responses.DiscussionThese results suggest that the specific acoustic contrasts associated with VNS can powerfully shape neural activity in the auditory pathway. Methods to promote plasticity in the central auditory system represent a new therapeutic avenue to treat auditory processing disorders. Understanding how different sound contrasts and neural activity patterns shape plasticity could have important clinical implications.https://www.frontiersin.org/articles/10.3389/fnins.2023.1248936/fullneuromodulationvagus nerve stimulationplasticityauditory cortexspeech
spellingShingle Michael S. Borland
Michael S. Borland
Elizabeth P. Buell
Elizabeth P. Buell
Jonathan R. Riley
Jonathan R. Riley
Alan M. Carroll
Alan M. Carroll
Nicole A. Moreno
Nicole A. Moreno
Pryanka Sharma
Pryanka Sharma
Katelyn M. Grasse
Katelyn M. Grasse
John M. Buell
John M. Buell
Michael P. Kilgard
Michael P. Kilgard
Crystal T. Engineer
Crystal T. Engineer
Precise sound characteristics drive plasticity in the primary auditory cortex with VNS-sound pairing
Frontiers in Neuroscience
neuromodulation
vagus nerve stimulation
plasticity
auditory cortex
speech
title Precise sound characteristics drive plasticity in the primary auditory cortex with VNS-sound pairing
title_full Precise sound characteristics drive plasticity in the primary auditory cortex with VNS-sound pairing
title_fullStr Precise sound characteristics drive plasticity in the primary auditory cortex with VNS-sound pairing
title_full_unstemmed Precise sound characteristics drive plasticity in the primary auditory cortex with VNS-sound pairing
title_short Precise sound characteristics drive plasticity in the primary auditory cortex with VNS-sound pairing
title_sort precise sound characteristics drive plasticity in the primary auditory cortex with vns sound pairing
topic neuromodulation
vagus nerve stimulation
plasticity
auditory cortex
speech
url https://www.frontiersin.org/articles/10.3389/fnins.2023.1248936/full
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