Binge Alcohol Drinking Alters Synaptic Processing of Executive and Emotional Information in Core Nucleus Accumbens Medium Spiny Neurons

The nucleus accumbens (NAc) is a forebrain region mediating the positive-reinforcing properties of drugs of abuse, including alcohol. It receives glutamatergic projections from multiple forebrain and limbic regions such as the prefrontal cortex (PFCx) and basolateral amygdala (BLA), respectively. Ho...

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Autores principales:	Jenya Kolpakova, Vincent van der Vinne, Pablo Giménez-Gómez, Timmy Le, In-Jee You, Rubing Zhao-Shea, Cristina Velazquez-Marrero, Andrew R. Tapper, Gilles E. Martin
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	nucleus accumbens decision making optogenetics binge alcohol drinking synaptic integration prefrontal cortex Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
Acceso en línea:	https://doaj.org/article/dd30f11b35e446e496adf5807da19d95
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spelling	oai:doaj.org-article:dd30f11b35e446e496adf5807da19d952021-11-16T06:26:27ZBinge Alcohol Drinking Alters Synaptic Processing of Executive and Emotional Information in Core Nucleus Accumbens Medium Spiny Neurons1662-510210.3389/fncel.2021.742207https://doaj.org/article/dd30f11b35e446e496adf5807da19d952021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fncel.2021.742207/fullhttps://doaj.org/toc/1662-5102The nucleus accumbens (NAc) is a forebrain region mediating the positive-reinforcing properties of drugs of abuse, including alcohol. It receives glutamatergic projections from multiple forebrain and limbic regions such as the prefrontal cortex (PFCx) and basolateral amygdala (BLA), respectively. However, it is unknown how NAc medium spiny neurons (MSNs) integrate PFCx and BLA inputs, and how this integration is affected by alcohol exposure. Because progress has been hampered by the inability to independently stimulate different pathways, we implemented a dual wavelength optogenetic approach to selectively and independently stimulate PFCx and BLA NAc inputs within the same brain slice. This approach functionally demonstrates that PFCx and BLA inputs synapse onto the same MSNs where they reciprocally inhibit each other pre-synaptically in a strict time-dependent manner. In alcohol-naïve mice, this temporal gating of BLA-inputs by PFCx afferents is stronger than the reverse, revealing that MSNs prioritize high-order executive processes information from the PFCx. Importantly, binge alcohol drinking alters this reciprocal inhibition by unilaterally strengthening BLA inhibition of PFCx inputs. In line with this observation, we demonstrate that in vivo optogenetic stimulation of the BLA, but not PFCx, blocks binge alcohol drinking escalation in mice. Overall, our results identify NAc MSNs as a key integrator of executive and emotional information and show that this integration is dysregulated during binge alcohol drinking.Jenya KolpakovaVincent van der VinnePablo Giménez-GómezTimmy LeIn-Jee YouRubing Zhao-SheaCristina Velazquez-MarreroAndrew R. TapperGilles E. MartinFrontiers Media S.A.articlenucleus accumbensdecision makingoptogeneticsbinge alcohol drinkingsynaptic integrationprefrontal cortexNeurosciences. Biological psychiatry. NeuropsychiatryRC321-571ENFrontiers in Cellular Neuroscience, Vol 15 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	nucleus accumbens decision making optogenetics binge alcohol drinking synaptic integration prefrontal cortex Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
spellingShingle	nucleus accumbens decision making optogenetics binge alcohol drinking synaptic integration prefrontal cortex Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 Jenya Kolpakova Vincent van der Vinne Pablo Giménez-Gómez Timmy Le In-Jee You Rubing Zhao-Shea Cristina Velazquez-Marrero Andrew R. Tapper Gilles E. Martin Binge Alcohol Drinking Alters Synaptic Processing of Executive and Emotional Information in Core Nucleus Accumbens Medium Spiny Neurons
description	The nucleus accumbens (NAc) is a forebrain region mediating the positive-reinforcing properties of drugs of abuse, including alcohol. It receives glutamatergic projections from multiple forebrain and limbic regions such as the prefrontal cortex (PFCx) and basolateral amygdala (BLA), respectively. However, it is unknown how NAc medium spiny neurons (MSNs) integrate PFCx and BLA inputs, and how this integration is affected by alcohol exposure. Because progress has been hampered by the inability to independently stimulate different pathways, we implemented a dual wavelength optogenetic approach to selectively and independently stimulate PFCx and BLA NAc inputs within the same brain slice. This approach functionally demonstrates that PFCx and BLA inputs synapse onto the same MSNs where they reciprocally inhibit each other pre-synaptically in a strict time-dependent manner. In alcohol-naïve mice, this temporal gating of BLA-inputs by PFCx afferents is stronger than the reverse, revealing that MSNs prioritize high-order executive processes information from the PFCx. Importantly, binge alcohol drinking alters this reciprocal inhibition by unilaterally strengthening BLA inhibition of PFCx inputs. In line with this observation, we demonstrate that in vivo optogenetic stimulation of the BLA, but not PFCx, blocks binge alcohol drinking escalation in mice. Overall, our results identify NAc MSNs as a key integrator of executive and emotional information and show that this integration is dysregulated during binge alcohol drinking.
format	article
author	Jenya Kolpakova Vincent van der Vinne Pablo Giménez-Gómez Timmy Le In-Jee You Rubing Zhao-Shea Cristina Velazquez-Marrero Andrew R. Tapper Gilles E. Martin
author_facet	Jenya Kolpakova Vincent van der Vinne Pablo Giménez-Gómez Timmy Le In-Jee You Rubing Zhao-Shea Cristina Velazquez-Marrero Andrew R. Tapper Gilles E. Martin
author_sort	Jenya Kolpakova
title	Binge Alcohol Drinking Alters Synaptic Processing of Executive and Emotional Information in Core Nucleus Accumbens Medium Spiny Neurons
title_short	Binge Alcohol Drinking Alters Synaptic Processing of Executive and Emotional Information in Core Nucleus Accumbens Medium Spiny Neurons
title_full	Binge Alcohol Drinking Alters Synaptic Processing of Executive and Emotional Information in Core Nucleus Accumbens Medium Spiny Neurons
title_fullStr	Binge Alcohol Drinking Alters Synaptic Processing of Executive and Emotional Information in Core Nucleus Accumbens Medium Spiny Neurons
title_full_unstemmed	Binge Alcohol Drinking Alters Synaptic Processing of Executive and Emotional Information in Core Nucleus Accumbens Medium Spiny Neurons
title_sort	binge alcohol drinking alters synaptic processing of executive and emotional information in core nucleus accumbens medium spiny neurons
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/dd30f11b35e446e496adf5807da19d95
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Binge Alcohol Drinking Alters Synaptic Processing of Executive and Emotional Information in Core Nucleus Accumbens Medium Spiny Neurons

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