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

Biology

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

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 (US)
Article number	2220
Journal	Nature communications
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-02365-8
State	Published - Dec 1 2017

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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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), [2220]. https://doi.org/10.1038/s41467-017-02365-8

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

In: Nature communications, Vol. 8, No. 1, 2220, 01.12.2017.

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

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

Juarez, Barbara ; Morel, Carole ; Ku, Stacy M. ; Liu, Yutong ; Zhang, Hongxing ; Montgomery, Sarah ; Gregoire, Hilledna ; Ribeiro, Efrain ; Crumiller, Marshall ; Roman-Ortiz, Ciorana ; Walsh, Jessica J. ; Jackson, Kelcy ; Croote, Denise E. ; Zhu, Yingbo ; Zhang, Song ; Vendruscolo, Leandro F. ; Edward, Scott ; Roberts, Amanda ; Hodes, Georgia E. ; Lu, Yongke ; Calipari, Erin S. ; Chaudhury, Dipesh ; Friedman, Allyson K. ; Han, Ming Hu. / Midbrain circuit regulation of individual alcohol drinking behaviors in mice. In: Nature communications. 2017 ; Vol. 8, No. 1.

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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 = "Funding Information: We thank G. F. Koob for his contribution on initial project design and continuing consultations; E. J. Nestler, S. J. Russo, R. C. Bagot, and E. A. Mouzon for their helpful discussions. We thank A. I. Cederbaum for his consultation on blood EtOH measurements. We would also like to thank the members of Icahn School of Medicine{\textquoteright}s Center for Comparative Medicine and Surgery for their efforts in maintaining our animals. This work was supported by National Institute of Health grants: AA022445 to M.-H.H.; T32 MH087004 and F31 AA022862 to B.J.; T32MH096678 and F31 MH108326 to S.M.K.; F32 MH096464 to A.K.F. This work was also supported by NARSAD Independent Investigator Award to M.-H.H. and the National Science Foundation in China award (NSFC-81200862) to H.Z. Publisher Copyright: {\textcopyright} 2017 The Author(s).",

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

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T1 - Midbrain circuit regulation of individual alcohol drinking behaviors in mice

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

N1 - Funding Information: We thank G. F. Koob for his contribution on initial project design and continuing consultations; E. J. Nestler, S. J. Russo, R. C. Bagot, and E. A. Mouzon for their helpful discussions. We thank A. I. Cederbaum for his consultation on blood EtOH measurements. We would also like to thank the members of Icahn School of Medicine’s Center for Comparative Medicine and Surgery for their efforts in maintaining our animals. This work was supported by National Institute of Health grants: AA022445 to M.-H.H.; T32 MH087004 and F31 AA022862 to B.J.; T32MH096678 and F31 MH108326 to S.M.K.; F32 MH096464 to A.K.F. This work was also supported by NARSAD Independent Investigator Award to M.-H.H. and the National Science Foundation in China award (NSFC-81200862) to H.Z. Publisher Copyright: © 2017 The Author(s).

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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JO - Nature Communications

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Midbrain circuit regulation of individual alcohol drinking behaviors in mice

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