Precise Sound Characteristics Drive Plasticity in the Primary Auditory Cortex with VNS-sound Pairing

Overview

Journal Front Neurosci

Date 2023 Sep 21

PMID 37732302

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

Affiliations

Soon will be listed here.

Abstract

Introduction: Repeatedly 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.

Methods: To 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.

Results: Pairing 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.

Discussion: These 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.

Citing Articles

Vagus nerve electrical stimulation in the recovery of upper limb motor functional impairment after ischemic stroke.

Chen L, Gao H, Wang Z, Gu B, Zhou W, Pang M Cogn Neurodyn. 2024; 18(5):3107-3124.

PMID: 39555282 PMC: 11564590. DOI: 10.1007/s11571-024-10143-8.

Pairing tones with vagus nerve stimulation improves brain stem responses to speech in the valproic acid model of autism.

Tamaoki Y, Pasapula V, Danaphongse T, Reyes A, Chandler C, Borland M J Neurophysiol. 2024; 132(5):1426-1436.

PMID: 39319784 PMC: 11573256. DOI: 10.1152/jn.00325.2024.

References

Meyers E, Solorzano B, James J, Ganzer P, Lai E, Rennaker 2nd R . Vagus Nerve Stimulation Enhances Stable Plasticity and Generalization of Stroke Recovery. Stroke. 2018; 49(3):710-717. PMC: 6454573. DOI: 10.1161/STROKEAHA.117.019202. View

Collins L, Boddington L, Steffan P, McCormick D . Vagus nerve stimulation induces widespread cortical and behavioral activation. Curr Biol. 2021; 31(10):2088-2098.e3. DOI: 10.1016/j.cub.2021.02.049. View

Edeline J, Manunta Y, Hennevin E . Induction of selective plasticity in the frequency tuning of auditory cortex and auditory thalamus neurons by locus coeruleus stimulation. Hear Res. 2010; 274(1-2):75-84. DOI: 10.1016/j.heares.2010.08.005. View

Lai J, David S . Short-Term Effects of Vagus Nerve Stimulation on Learning and Evoked Activity in Auditory Cortex. eNeuro. 2021; 8(3). PMC: 8240839. DOI: 10.1523/ENEURO.0522-20.2021. View

Kilgard M, Merzenich M . Cortical map reorganization enabled by nucleus basalis activity. Science. 1998; 279(5357):1714-8. DOI: 10.1126/science.279.5357.1714. View

Reed A, Riley J, Carraway R, Carrasco A, Perez C, Jakkamsetti V . Cortical map plasticity improves learning but is not necessary for improved performance. Neuron. 2011; 70(1):121-31. DOI: 10.1016/j.neuron.2011.02.038. View

Souza R, Oleksiak C, Tabet M, Rennaker R, Hays S, Kilgard M . Vagus nerve stimulation promotes extinction generalization across sensory modalities. Neurobiol Learn Mem. 2021; 181:107425. DOI: 10.1016/j.nlm.2021.107425. View

Engineer C, Hays S, Kilgard M . Vagus nerve stimulation as a potential adjuvant to behavioral therapy for autism and other neurodevelopmental disorders. J Neurodev Disord. 2017; 9:20. PMC: 5496407. DOI: 10.1186/s11689-017-9203-z. View

Hulsey D, Shedd C, Sarker S, Kilgard M, Hays S . Norepinephrine and serotonin are required for vagus nerve stimulation directed cortical plasticity. Exp Neurol. 2019; 320:112975. PMC: 6708444. DOI: 10.1016/j.expneurol.2019.112975. View

10.

Borland M, Engineer C, Vrana W, Moreno N, Engineer N, Vanneste S . The Interval Between VNS-Tone Pairings Determines the Extent of Cortical Map Plasticity. Neuroscience. 2017; 369:76-86. PMC: 5766390. DOI: 10.1016/j.neuroscience.2017.11.004. View

11.

Rabinovich R, Kato D, Bruno R . Learning enhances encoding of time and temporal surprise in mouse primary sensory cortex. Nat Commun. 2022; 13(1):5504. PMC: 9489862. DOI: 10.1038/s41467-022-33141-y. View

12.

Buell E, Borland M, Loerwald K, Chandler C, Hays S, Engineer C . Vagus Nerve Stimulation Rate and Duration Determine whether Sensory Pairing Produces Neural Plasticity. Neuroscience. 2019; 406:290-299. PMC: 6511481. DOI: 10.1016/j.neuroscience.2019.03.019. View

13.

Fremaux N, Gerstner W . Neuromodulated Spike-Timing-Dependent Plasticity, and Theory of Three-Factor Learning Rules. Front Neural Circuits. 2016; 9:85. PMC: 4717313. DOI: 10.3389/fncir.2015.00085. View

14.

Raizada R, Tsao F, Liu H, Kuhl P . Quantifying the adequacy of neural representations for a cross-language phonetic discrimination task: prediction of individual differences. Cereb Cortex. 2009; 20(1):1-12. PMC: 2860710. DOI: 10.1093/cercor/bhp076. View

15.

Ma X, Suga N . Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. J Neurophysiol. 2003; 89(1):90-103. DOI: 10.1152/jn.00968.2001. View

16.

Takahashi H, Yokota R, Funamizu A, Kose H, Kanzaki R . Learning-stage-dependent, field-specific, map plasticity in the rat auditory cortex during appetitive operant conditioning. Neuroscience. 2011; 199:243-58. DOI: 10.1016/j.neuroscience.2011.09.046. View

17.

Borland M, Vrana W, Moreno N, Fogarty E, Buell E, Sharma P . Cortical Map Plasticity as a Function of Vagus Nerve Stimulation Intensity. Brain Stimul. 2015; 9(1):117-23. PMC: 4724352. DOI: 10.1016/j.brs.2015.08.018. View

18.

Adcock K, Chandler C, Buell E, Solorzano B, Loerwald K, Borland M . Vagus nerve stimulation paired with tones restores auditory processing in a rat model of Rett syndrome. Brain Stimul. 2020; 13(6):1494-1503. DOI: 10.1016/j.brs.2020.08.006. View

19.

Hulsey D, Riley J, Loerwald K, Rennaker 2nd R, Kilgard M, Hays S . Parametric characterization of neural activity in the locus coeruleus in response to vagus nerve stimulation. Exp Neurol. 2016; 289:21-30. PMC: 5297969. DOI: 10.1016/j.expneurol.2016.12.005. View

20.

Moucha R, Pandya P, Engineer N, Rathbun D, Kilgard M . Background sounds contribute to spectrotemporal plasticity in primary auditory cortex. Exp Brain Res. 2004; 162(4):417-27. PMC: 2950066. DOI: 10.1007/s00221-004-2098-4. View