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Adult Plasticity in the Subcortical Auditory Pathway of the Maternal Mouse

Subcortical auditory nuclei were traditionally viewed as non-plastic in adulthood so that acoustic information could be stably conveyed to higher auditory areas. Studies in a variety of species, including humans, now suggest that prolonged acoustic training can drive long-lasting brainstem plasticit...

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Autores principales: Miranda, Jason A., Shepard, Kathryn N., McClintock, Shannon K., Liu, Robert C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4081580/
https://www.ncbi.nlm.nih.gov/pubmed/24992362
http://dx.doi.org/10.1371/journal.pone.0101630
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author Miranda, Jason A.
Shepard, Kathryn N.
McClintock, Shannon K.
Liu, Robert C.
author_facet Miranda, Jason A.
Shepard, Kathryn N.
McClintock, Shannon K.
Liu, Robert C.
author_sort Miranda, Jason A.
collection PubMed
description Subcortical auditory nuclei were traditionally viewed as non-plastic in adulthood so that acoustic information could be stably conveyed to higher auditory areas. Studies in a variety of species, including humans, now suggest that prolonged acoustic training can drive long-lasting brainstem plasticity. The neurobiological mechanisms for such changes are not well understood in natural behavioral contexts due to a relative dearth of in vivo animal models in which to study this. Here, we demonstrate in a mouse model that a natural life experience with increased demands on the auditory system – motherhood – is associated with improved temporal processing in the subcortical auditory pathway. We measured the auditory brainstem response to test whether mothers and pup-naïve virgin mice differed in temporal responses to both broadband and tone stimuli, including ultrasonic frequencies found in mouse pup vocalizations. Mothers had shorter latencies for early ABR peaks, indicating plasticity in the auditory nerve and the cochlear nucleus. Shorter interpeak latency between waves IV and V also suggest plasticity in the inferior colliculus. Hormone manipulations revealed that these cannot be explained solely by estrogen levels experienced during pregnancy and parturition in mothers. In contrast, we found that pup-care experience, independent of pregnancy and parturition, contributes to shortening auditory brainstem response latencies. These results suggest that acoustic experience in the maternal context imparts plasticity on early auditory processing that lasts beyond pup weaning. In addition to establishing an animal model for exploring adult auditory brainstem plasticity in a neuroethological context, our results have broader implications for models of perceptual, behavioral and neural changes that arise during maternity, where subcortical sensorineural plasticity has not previously been considered.
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spelling pubmed-40815802014-07-10 Adult Plasticity in the Subcortical Auditory Pathway of the Maternal Mouse Miranda, Jason A. Shepard, Kathryn N. McClintock, Shannon K. Liu, Robert C. PLoS One Research Article Subcortical auditory nuclei were traditionally viewed as non-plastic in adulthood so that acoustic information could be stably conveyed to higher auditory areas. Studies in a variety of species, including humans, now suggest that prolonged acoustic training can drive long-lasting brainstem plasticity. The neurobiological mechanisms for such changes are not well understood in natural behavioral contexts due to a relative dearth of in vivo animal models in which to study this. Here, we demonstrate in a mouse model that a natural life experience with increased demands on the auditory system – motherhood – is associated with improved temporal processing in the subcortical auditory pathway. We measured the auditory brainstem response to test whether mothers and pup-naïve virgin mice differed in temporal responses to both broadband and tone stimuli, including ultrasonic frequencies found in mouse pup vocalizations. Mothers had shorter latencies for early ABR peaks, indicating plasticity in the auditory nerve and the cochlear nucleus. Shorter interpeak latency between waves IV and V also suggest plasticity in the inferior colliculus. Hormone manipulations revealed that these cannot be explained solely by estrogen levels experienced during pregnancy and parturition in mothers. In contrast, we found that pup-care experience, independent of pregnancy and parturition, contributes to shortening auditory brainstem response latencies. These results suggest that acoustic experience in the maternal context imparts plasticity on early auditory processing that lasts beyond pup weaning. In addition to establishing an animal model for exploring adult auditory brainstem plasticity in a neuroethological context, our results have broader implications for models of perceptual, behavioral and neural changes that arise during maternity, where subcortical sensorineural plasticity has not previously been considered. Public Library of Science 2014-07-03 /pmc/articles/PMC4081580/ /pubmed/24992362 http://dx.doi.org/10.1371/journal.pone.0101630 Text en © 2014 Miranda et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Miranda, Jason A.
Shepard, Kathryn N.
McClintock, Shannon K.
Liu, Robert C.
Adult Plasticity in the Subcortical Auditory Pathway of the Maternal Mouse
title Adult Plasticity in the Subcortical Auditory Pathway of the Maternal Mouse
title_full Adult Plasticity in the Subcortical Auditory Pathway of the Maternal Mouse
title_fullStr Adult Plasticity in the Subcortical Auditory Pathway of the Maternal Mouse
title_full_unstemmed Adult Plasticity in the Subcortical Auditory Pathway of the Maternal Mouse
title_short Adult Plasticity in the Subcortical Auditory Pathway of the Maternal Mouse
title_sort adult plasticity in the subcortical auditory pathway of the maternal mouse
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4081580/
https://www.ncbi.nlm.nih.gov/pubmed/24992362
http://dx.doi.org/10.1371/journal.pone.0101630
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