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Arousal State-Dependent Alterations in VTA-GABAergic Neuronal Activity
Decades of research have implicated the ventral tegmental area (VTA) in motivation, learning and reward processing. We and others recently demonstrated that it also serves as an important node in sleep/wake regulation. Specifically, VTA-dopaminergic neuron activation is sufficient to drive wakefulne...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Society for Neuroscience
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7218005/ https://www.ncbi.nlm.nih.gov/pubmed/32054621 http://dx.doi.org/10.1523/ENEURO.0356-19.2020 |
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author | Eban-Rothschild, Ada Borniger, Jeremy C. Rothschild, Gideon Giardino, William J. Morrow, Joshua G. de Lecea, Luis |
author_facet | Eban-Rothschild, Ada Borniger, Jeremy C. Rothschild, Gideon Giardino, William J. Morrow, Joshua G. de Lecea, Luis |
author_sort | Eban-Rothschild, Ada |
collection | PubMed |
description | Decades of research have implicated the ventral tegmental area (VTA) in motivation, learning and reward processing. We and others recently demonstrated that it also serves as an important node in sleep/wake regulation. Specifically, VTA-dopaminergic neuron activation is sufficient to drive wakefulness and necessary for the maintenance of wakefulness. However, the role of VTA-GABAergic neurons in arousal regulation is not fully understood. It is still unclear whether VTA-GABAergic neurons predictably alter their activity across arousal states, what is the nature of interactions between VTA-GABAergic activity and cortical oscillations, and how activity in VTA-GABAergic neurons relates to VTA-dopaminergic neurons in the context of sleep/wake regulation. To address these, we simultaneously recorded population activity from VTA subpopulations and electroencephalography/electromyography (EEG/EMG) signals during spontaneous sleep/wake states and in the presence of salient stimuli in freely-behaving mice. We found that VTA-GABAergic neurons exhibit robust arousal-state-dependent alterations in population activity, with high activity and transients during wakefulness and REM sleep. During wakefulness, population activity of VTA-GABAergic neurons, but not VTA-dopaminergic neurons, was positively correlated with EEG γ power and negatively correlated with θ power. During NREM sleep, population activity in both VTA-GABAergic and VTA-dopaminergic neurons negatively correlated with δ, θ, and σ power bands. Salient stimuli, with both positive and negative valence, activated VTA-GABAergic neurons. Together, our data indicate that VTA-GABAergic neurons, like their dopaminergic counterparts, drastically alter their activity across sleep-wake states. Changes in their activity predicts cortical oscillatory patterns reflected in the EEG, which are distinct from EEG spectra associated with dopaminergic neural activity. |
format | Online Article Text |
id | pubmed-7218005 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Society for Neuroscience |
record_format | MEDLINE/PubMed |
spelling | pubmed-72180052020-05-13 Arousal State-Dependent Alterations in VTA-GABAergic Neuronal Activity Eban-Rothschild, Ada Borniger, Jeremy C. Rothschild, Gideon Giardino, William J. Morrow, Joshua G. de Lecea, Luis eNeuro Research Article: Confirmation Decades of research have implicated the ventral tegmental area (VTA) in motivation, learning and reward processing. We and others recently demonstrated that it also serves as an important node in sleep/wake regulation. Specifically, VTA-dopaminergic neuron activation is sufficient to drive wakefulness and necessary for the maintenance of wakefulness. However, the role of VTA-GABAergic neurons in arousal regulation is not fully understood. It is still unclear whether VTA-GABAergic neurons predictably alter their activity across arousal states, what is the nature of interactions between VTA-GABAergic activity and cortical oscillations, and how activity in VTA-GABAergic neurons relates to VTA-dopaminergic neurons in the context of sleep/wake regulation. To address these, we simultaneously recorded population activity from VTA subpopulations and electroencephalography/electromyography (EEG/EMG) signals during spontaneous sleep/wake states and in the presence of salient stimuli in freely-behaving mice. We found that VTA-GABAergic neurons exhibit robust arousal-state-dependent alterations in population activity, with high activity and transients during wakefulness and REM sleep. During wakefulness, population activity of VTA-GABAergic neurons, but not VTA-dopaminergic neurons, was positively correlated with EEG γ power and negatively correlated with θ power. During NREM sleep, population activity in both VTA-GABAergic and VTA-dopaminergic neurons negatively correlated with δ, θ, and σ power bands. Salient stimuli, with both positive and negative valence, activated VTA-GABAergic neurons. Together, our data indicate that VTA-GABAergic neurons, like their dopaminergic counterparts, drastically alter their activity across sleep-wake states. Changes in their activity predicts cortical oscillatory patterns reflected in the EEG, which are distinct from EEG spectra associated with dopaminergic neural activity. Society for Neuroscience 2020-03-30 /pmc/articles/PMC7218005/ /pubmed/32054621 http://dx.doi.org/10.1523/ENEURO.0356-19.2020 Text en Copyright © 2020 Eban-Rothschild et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. |
spellingShingle | Research Article: Confirmation Eban-Rothschild, Ada Borniger, Jeremy C. Rothschild, Gideon Giardino, William J. Morrow, Joshua G. de Lecea, Luis Arousal State-Dependent Alterations in VTA-GABAergic Neuronal Activity |
title | Arousal State-Dependent Alterations in VTA-GABAergic Neuronal Activity |
title_full | Arousal State-Dependent Alterations in VTA-GABAergic Neuronal Activity |
title_fullStr | Arousal State-Dependent Alterations in VTA-GABAergic Neuronal Activity |
title_full_unstemmed | Arousal State-Dependent Alterations in VTA-GABAergic Neuronal Activity |
title_short | Arousal State-Dependent Alterations in VTA-GABAergic Neuronal Activity |
title_sort | arousal state-dependent alterations in vta-gabaergic neuronal activity |
topic | Research Article: Confirmation |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7218005/ https://www.ncbi.nlm.nih.gov/pubmed/32054621 http://dx.doi.org/10.1523/ENEURO.0356-19.2020 |
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