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 & 4 others Erin S. Calipari, Dipesh Chaudhury, Allyson K. Friedman, Ming Hu Han

    Research output: Contribution to journalArticle

    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 languageEnglish (US)
    Article number2220
    JournalNature Communications
    Volume8
    Issue number1
    DOIs
    StatePublished - Dec 1 2017

    Fingerprint

    Drinking Behavior
    drinking
    Mesencephalon
    Alcohol Drinking
    mice
    alcohols
    Alcohols
    Ventral Tegmental Area
    Networks (circuits)
    Dopaminergic Neurons
    neurons
    dopamine
    Neurons
    Dopamine
    bursts
    disorders
    Nucleus Accumbens
    Substance-Related Disorders

    ASJC Scopus subject areas

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

    Cite this

    Juarez, B., Morel, C., Ku, S. M., Liu, Y., Zhang, H., Montgomery, S., ... 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 journalArticle

    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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