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Cross-species conservation in the regulation of parvalbumin by perineuronal nets

Parvalbumin (PV) neurons play an integral role in regulating neural dynamics and plasticity. Therefore, understanding the factors that regulate PV expression is important for revealing modulators of brain function. While the contribution of PV neurons to neural processes has been studied in mammals,...

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Autores principales: Wang, Angela S., Wan, Xinghaoyun, Storch, Daria-Salina, Cornez, Gilles, Balthazart, Jacques, Cisneros-Franco, J. Miguel, de Villers-Sidani, Etienne, Sakata, Jon T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10515890/
https://www.ncbi.nlm.nih.gov/pubmed/37745532
http://dx.doi.org/10.1101/2023.09.13.557580
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author Wang, Angela S.
Wan, Xinghaoyun
Storch, Daria-Salina
Cornez, Gilles
Balthazart, Jacques
Cisneros-Franco, J. Miguel
de Villers-Sidani, Etienne
Sakata, Jon T.
author_facet Wang, Angela S.
Wan, Xinghaoyun
Storch, Daria-Salina
Cornez, Gilles
Balthazart, Jacques
Cisneros-Franco, J. Miguel
de Villers-Sidani, Etienne
Sakata, Jon T.
author_sort Wang, Angela S.
collection PubMed
description Parvalbumin (PV) neurons play an integral role in regulating neural dynamics and plasticity. Therefore, understanding the factors that regulate PV expression is important for revealing modulators of brain function. While the contribution of PV neurons to neural processes has been studied in mammals, relatively little is known about PV function in non-mammalian species, and discerning similarities in the regulation of PV across species can provide insight into evolutionary conservation in the role of PV neurons. Here we investigated factors that affect the abundance of PV in PV neurons in sensory and motor circuits of songbirds and rodents. In particular, we examined the degree to which perineuronal nets (PNNs), extracellular matrices that preferentially surround PV neurons, modulate PV abundance as well as how the relationship between PV and PNN expression differs across brain areas and species and changes over development. We generally found that cortical PV neurons that are surrounded by PNNs (PV+PNN neurons) are more enriched with PV than PV neurons without PNNs (PV-PNN neurons) across both rodents and songbirds. Interestingly, the relationship between PV and PNN expression in the vocal portion of the basal ganglia of songbirds (Area X) differed from that in other areas, with PV+PNN neurons having lower PV expression compared to PV-PNN neurons. These relationships remained consistent across development in vocal motor circuits of the songbird brain. Finally, we discovered a causal contribution of PNNs to PV expression in songbirds because degradation of PNNs led to a diminution of PV expression in PV neurons. These findings in reveal a conserved relationship between PV and PNN expression in sensory and motor cortices and across songbirds and rodents and suggest that PV neurons could modulate plasticity and neural dynamics in similar ways across songbirds and rodents.
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spelling pubmed-105158902023-09-23 Cross-species conservation in the regulation of parvalbumin by perineuronal nets Wang, Angela S. Wan, Xinghaoyun Storch, Daria-Salina Cornez, Gilles Balthazart, Jacques Cisneros-Franco, J. Miguel de Villers-Sidani, Etienne Sakata, Jon T. bioRxiv Article Parvalbumin (PV) neurons play an integral role in regulating neural dynamics and plasticity. Therefore, understanding the factors that regulate PV expression is important for revealing modulators of brain function. While the contribution of PV neurons to neural processes has been studied in mammals, relatively little is known about PV function in non-mammalian species, and discerning similarities in the regulation of PV across species can provide insight into evolutionary conservation in the role of PV neurons. Here we investigated factors that affect the abundance of PV in PV neurons in sensory and motor circuits of songbirds and rodents. In particular, we examined the degree to which perineuronal nets (PNNs), extracellular matrices that preferentially surround PV neurons, modulate PV abundance as well as how the relationship between PV and PNN expression differs across brain areas and species and changes over development. We generally found that cortical PV neurons that are surrounded by PNNs (PV+PNN neurons) are more enriched with PV than PV neurons without PNNs (PV-PNN neurons) across both rodents and songbirds. Interestingly, the relationship between PV and PNN expression in the vocal portion of the basal ganglia of songbirds (Area X) differed from that in other areas, with PV+PNN neurons having lower PV expression compared to PV-PNN neurons. These relationships remained consistent across development in vocal motor circuits of the songbird brain. Finally, we discovered a causal contribution of PNNs to PV expression in songbirds because degradation of PNNs led to a diminution of PV expression in PV neurons. These findings in reveal a conserved relationship between PV and PNN expression in sensory and motor cortices and across songbirds and rodents and suggest that PV neurons could modulate plasticity and neural dynamics in similar ways across songbirds and rodents. Cold Spring Harbor Laboratory 2023-09-13 /pmc/articles/PMC10515890/ /pubmed/37745532 http://dx.doi.org/10.1101/2023.09.13.557580 Text en https://creativecommons.org/licenses/by-nd/4.0/This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, and only so long as attribution is given to the creator. The license allows for commercial use.
spellingShingle Article
Wang, Angela S.
Wan, Xinghaoyun
Storch, Daria-Salina
Cornez, Gilles
Balthazart, Jacques
Cisneros-Franco, J. Miguel
de Villers-Sidani, Etienne
Sakata, Jon T.
Cross-species conservation in the regulation of parvalbumin by perineuronal nets
title Cross-species conservation in the regulation of parvalbumin by perineuronal nets
title_full Cross-species conservation in the regulation of parvalbumin by perineuronal nets
title_fullStr Cross-species conservation in the regulation of parvalbumin by perineuronal nets
title_full_unstemmed Cross-species conservation in the regulation of parvalbumin by perineuronal nets
title_short Cross-species conservation in the regulation of parvalbumin by perineuronal nets
title_sort cross-species conservation in the regulation of parvalbumin by perineuronal nets
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10515890/
https://www.ncbi.nlm.nih.gov/pubmed/37745532
http://dx.doi.org/10.1101/2023.09.13.557580
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