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Voluntary alcohol consumption disrupts coupling of prefrontal cortical activity to arousal

View ORCID ProfileGrayson Sipe, Ivan Linares-Garcia, My Nguyen, Elena Vazey, View ORCID ProfileRafiq Huda
doi: https://doi.org/10.1101/2021.02.01.429229
Grayson Sipe
1Department of Brain and Cognitive Science, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge United States
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Ivan Linares-Garcia
2WM Keck Center for Collaborative Neuroscience, Department of Cell Biology and Neuroscience, Rutgers University – New Brunswick, Piscataway United States
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My Nguyen
2WM Keck Center for Collaborative Neuroscience, Department of Cell Biology and Neuroscience, Rutgers University – New Brunswick, Piscataway United States
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Elena Vazey
3Department of Biology, The University of Massachusetts, Amherst United States
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Rafiq Huda
2WM Keck Center for Collaborative Neuroscience, Department of Cell Biology and Neuroscience, Rutgers University – New Brunswick, Piscataway United States
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  • For correspondence: rafiq.huda@rutgers.edu
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Abstract

Alcohol use disorder (AUD) exacts a major personal, societal, and economic toll. Top-down control from the prefrontal cortex (PFC), a critical hub for decision making, executive, and other cognitive functions, is key for the regulation of alcohol consumption. Arousal exerts profound effects on cortical processing, allowing it to potentially modulate PFC functions relevant for alcohol consumption and AUD. Despite this, it is unclear whether and how arousal-mediated modulation of PFC circuits relates to voluntary alcohol drinking behaviors. Two-photon microscopy is ideally suited for dissecting the neural circuit mechanisms underlying the effect of alcohol on intact circuits in behaving animals. We addressed a major limitation of this technology by developing a novel behavioral paradigm for voluntary drinking in head-fixed mice. We recorded responses of layer 2/3 excitatory neurons in the anterior cingulate cortex (ACC) subdivision of the PFC as mice voluntarily consumed ethanol, along with video recording of the pupil to track momentary fluctuations in arousal. Ethanol consumption bidirectionally modified the activity of subsets of ACC neurons, both at slow (minutes) and fast (sub-second) time scales. Remarkably, we found that the coupling of arousal to ACC activity before drinking was associated with subsequent ethanol engagement behavior. In turn, ethanol consumption modulated neuronal-arousal coupling. Together, our results suggest neuronal-arousal coupling as a key biomarker for alcohol drinking and lays the groundwork for future studies to dissect the therapeutic potential of this process for AUD and other substance use disorders.

Competing Interest Statement

The authors have declared no competing interest.

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Posted February 02, 2021.
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Voluntary alcohol consumption disrupts coupling of prefrontal cortical activity to arousal
Grayson Sipe, Ivan Linares-Garcia, My Nguyen, Elena Vazey, Rafiq Huda
bioRxiv 2021.02.01.429229; doi: https://doi.org/10.1101/2021.02.01.429229
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Voluntary alcohol consumption disrupts coupling of prefrontal cortical activity to arousal
Grayson Sipe, Ivan Linares-Garcia, My Nguyen, Elena Vazey, Rafiq Huda
bioRxiv 2021.02.01.429229; doi: https://doi.org/10.1101/2021.02.01.429229

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