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

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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10.1038/s41467-017-02365-8

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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

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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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.",

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