Midbrain circuit regulation of individual alcohol drinking behaviors in mice

Barbara Juarez; Carole Morel; Stacy M. Ku; Yutong Liu; Hongxing Zhang; Sarah Montgomery; Hilledna Gregoire; Efrain Ribeiro; Marshall Crumiller; Ciorana Roman-Ortiz; Jessica J. Walsh; Kelcy Jackson; Denise E. Croote; Yingbo Zhu; Song Zhang; Leandro F. Vendruscolo; Scott Edward; Amanda Roberts; Georgia E. Hodes; Yongke Lu; Erin S. Calipari; Dipesh Chaudhury; Allyson K. Friedman; Ming Hu Han

doi:10.1038/s41467-017-02365-8

Midbrain circuit regulation of individual alcohol drinking behaviors in mice

Barbara Juarez, Carole Morel, Stacy M. Ku, Yutong Liu, Hongxing Zhang, Sarah Montgomery, Hilledna Gregoire, Efrain Ribeiro, Marshall Crumiller, Ciorana Roman-Ortiz, Jessica J. Walsh, Kelcy Jackson, Denise E. Croote, Yingbo Zhu, Song Zhang, Leandro F. Vendruscolo, Scott Edward, Amanda Roberts, Georgia E. Hodes, Yongke LuErin S. Calipari, Dipesh Chaudhury, Allyson K. Friedman, Ming Hu Han

Research output: Contribution to journal › Article › peer-review

57 Scopus citations

Abstract

Alcohol-use disorder (AUD) is the most prevalent substance-use disorder worldwide. There is substantial individual variability in alcohol drinking behaviors in the population, the neural circuit mechanisms of which remain elusive. Utilizing in vivo electrophysiological techniques, we find that low alcohol drinking (LAD) mice have dramatically higher ventral tegmental area (VTA) dopamine neuron firing and burst activity. Unexpectedly, VTA dopamine neuron activity in high alcohol drinking (HAD) mice does not differ from alcohol naive mice. Optogenetically enhancing VTA dopamine neuron burst activity in HAD mice decreases alcohol drinking behaviors. Circuit-specific recordings reveal that spontaneous activity of nucleus accumbens-projecting VTA (VTA-NAc) neurons is selectively higher in LAD mice. Specifically activating this projection is sufficient to reduce alcohol consumption in HAD mice. Furthermore, we uncover ionic and cellular mechanisms that suggest unique neuroadaptations between the alcohol drinking groups. Together, these data identify a neural circuit responsible for individual alcohol drinking behaviors.

Original language	English
Article number	2220
Journal	Nature Communications
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-02365-8
State	Published - 1 Dec 2017

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Juarez, B., Morel, C., Ku, S. M., Liu, Y., Zhang, H., Montgomery, S., Gregoire, H., Ribeiro, E., Crumiller, M., Roman-Ortiz, C., Walsh, J. J., Jackson, K., Croote, D. E., Zhu, Y., Zhang, S., Vendruscolo, L. F., Edward, S., Roberts, A., Hodes, G. E., ... Han, M. H. (2017). Midbrain circuit regulation of individual alcohol drinking behaviors in mice. Nature Communications, 8(1), Article 2220. https://doi.org/10.1038/s41467-017-02365-8

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title = "Midbrain circuit regulation of individual alcohol drinking behaviors in mice",

abstract = "Alcohol-use disorder (AUD) is the most prevalent substance-use disorder worldwide. There is substantial individual variability in alcohol drinking behaviors in the population, the neural circuit mechanisms of which remain elusive. Utilizing in vivo electrophysiological techniques, we find that low alcohol drinking (LAD) mice have dramatically higher ventral tegmental area (VTA) dopamine neuron firing and burst activity. Unexpectedly, VTA dopamine neuron activity in high alcohol drinking (HAD) mice does not differ from alcohol naive mice. Optogenetically enhancing VTA dopamine neuron burst activity in HAD mice decreases alcohol drinking behaviors. Circuit-specific recordings reveal that spontaneous activity of nucleus accumbens-projecting VTA (VTA-NAc) neurons is selectively higher in LAD mice. Specifically activating this projection is sufficient to reduce alcohol consumption in HAD mice. Furthermore, we uncover ionic and cellular mechanisms that suggest unique neuroadaptations between the alcohol drinking groups. Together, these data identify a neural circuit responsible for individual alcohol drinking behaviors.",

author = "Barbara Juarez and Carole Morel and Ku, {Stacy M.} and Yutong Liu and Hongxing Zhang and Sarah Montgomery and Hilledna Gregoire and Efrain Ribeiro and Marshall Crumiller and Ciorana Roman-Ortiz and Walsh, {Jessica J.} and Kelcy Jackson and Croote, {Denise E.} and Yingbo Zhu and Song Zhang and Vendruscolo, {Leandro F.} and Scott Edward and Amanda Roberts and Hodes, {Georgia E.} and Yongke Lu and Calipari, {Erin S.} and Dipesh Chaudhury and Friedman, {Allyson K.} and Han, {Ming Hu}",

note = "Publisher Copyright: {\textcopyright} 2017 The Author(s).",

year = "2017",

month = dec,

day = "1",

doi = "10.1038/s41467-017-02365-8",

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Juarez, B, Morel, C, Ku, SM, Liu, Y, Zhang, H, Montgomery, S, Gregoire, H, Ribeiro, E, Crumiller, M, Roman-Ortiz, C, Walsh, JJ, Jackson, K, Croote, DE, Zhu, Y, Zhang, S, Vendruscolo, LF, Edward, S, Roberts, A, Hodes, GE, Lu, Y, Calipari, ES, Chaudhury, D, Friedman, AK & Han, MH 2017, 'Midbrain circuit regulation of individual alcohol drinking behaviors in mice', Nature Communications, vol. 8, no. 1, 2220. https://doi.org/10.1038/s41467-017-02365-8

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AU - Juarez, Barbara

AU - Morel, Carole

AU - Ku, Stacy M.

AU - Liu, Yutong

AU - Zhang, Hongxing

AU - Montgomery, Sarah

AU - Gregoire, Hilledna

AU - Ribeiro, Efrain

AU - Crumiller, Marshall

AU - Roman-Ortiz, Ciorana

AU - Walsh, Jessica J.

AU - Jackson, Kelcy

AU - Croote, Denise E.

AU - Zhu, Yingbo

AU - Zhang, Song

AU - Vendruscolo, Leandro F.

AU - Edward, Scott

AU - Roberts, Amanda

AU - Hodes, Georgia E.

AU - Lu, Yongke

AU - Calipari, Erin S.

AU - Chaudhury, Dipesh

AU - Friedman, Allyson K.

AU - Han, Ming Hu

PY - 2017/12/1

Y1 - 2017/12/1

N2 - Alcohol-use disorder (AUD) is the most prevalent substance-use disorder worldwide. There is substantial individual variability in alcohol drinking behaviors in the population, the neural circuit mechanisms of which remain elusive. Utilizing in vivo electrophysiological techniques, we find that low alcohol drinking (LAD) mice have dramatically higher ventral tegmental area (VTA) dopamine neuron firing and burst activity. Unexpectedly, VTA dopamine neuron activity in high alcohol drinking (HAD) mice does not differ from alcohol naive mice. Optogenetically enhancing VTA dopamine neuron burst activity in HAD mice decreases alcohol drinking behaviors. Circuit-specific recordings reveal that spontaneous activity of nucleus accumbens-projecting VTA (VTA-NAc) neurons is selectively higher in LAD mice. Specifically activating this projection is sufficient to reduce alcohol consumption in HAD mice. Furthermore, we uncover ionic and cellular mechanisms that suggest unique neuroadaptations between the alcohol drinking groups. Together, these data identify a neural circuit responsible for individual alcohol drinking behaviors.

AB - Alcohol-use disorder (AUD) is the most prevalent substance-use disorder worldwide. There is substantial individual variability in alcohol drinking behaviors in the population, the neural circuit mechanisms of which remain elusive. Utilizing in vivo electrophysiological techniques, we find that low alcohol drinking (LAD) mice have dramatically higher ventral tegmental area (VTA) dopamine neuron firing and burst activity. Unexpectedly, VTA dopamine neuron activity in high alcohol drinking (HAD) mice does not differ from alcohol naive mice. Optogenetically enhancing VTA dopamine neuron burst activity in HAD mice decreases alcohol drinking behaviors. Circuit-specific recordings reveal that spontaneous activity of nucleus accumbens-projecting VTA (VTA-NAc) neurons is selectively higher in LAD mice. Specifically activating this projection is sufficient to reduce alcohol consumption in HAD mice. Furthermore, we uncover ionic and cellular mechanisms that suggest unique neuroadaptations between the alcohol drinking groups. Together, these data identify a neural circuit responsible for individual alcohol drinking behaviors.

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SN - 2041-1723

VL - 8

JO - Nature Communications

JF - Nature Communications

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ER -

Midbrain circuit regulation of individual alcohol drinking behaviors in mice

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