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Hippocampal Input to the Nucleus Accumbens Shell Enhances Food Palatability

  • Angela K. Yang
    Affiliations
    Integrated Program in Neuroscience, McGill University, Montreal, Quebec, Canada

    Center for Studies in Behavioral Neurobiology, Concordia University, Montreal, Quebec, Canada
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  • Jesse A. Mendoza
    Affiliations
    Department of Psychology, McGill University, Montreal, Quebec, Canada

    Center for Studies in Behavioral Neurobiology, Concordia University, Montreal, Quebec, Canada
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  • Christopher K. Lafferty
    Affiliations
    Department of Psychology, McGill University, Montreal, Quebec, Canada

    Center for Studies in Behavioral Neurobiology, Concordia University, Montreal, Quebec, Canada
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  • Franca Lacroix
    Affiliations
    Department of Psychology, McGill University, Montreal, Quebec, Canada
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  • Jonathan P. Britt
    Correspondence
    Address correspondence to Jonathan Britt, Ph.D., McGill University, Stewart Biology Building, 1205 Docteur Penfield Ave., Montreal, QC H3A 1B1, Canada.
    Affiliations
    Integrated Program in Neuroscience, McGill University, Montreal, Quebec, Canada

    Department of Psychology, McGill University, Montreal, Quebec, Canada

    Center for Studies in Behavioral Neurobiology, Concordia University, Montreal, Quebec, Canada
    Search for articles by this author
Published:September 19, 2019DOI:https://doi.org/10.1016/j.biopsych.2019.09.007

      Abstract

      Background

      Insight into the neural basis of hedonic processing has come from studies of food palatability in rodents. Pharmacological manipulations of the nucleus accumbens shell (NAcSh) have repeatedly been demonstrated to increase hedonic taste reactivity, yet the contribution of specific NAcSh circuit components is unknown.

      Methods

      Bidirectional optogenetic manipulations were targeted to the principal NAcSh projection neurons and afferent pathways in mice during free feeding assays. Number of licks per bout of consumption was used as a measure of food palatability as it was confirmed to track sucrose concentration and subjective flavor preferences.

      Results

      Photoinhibition of NAcSh neurons, whether general or cell-type specific, was found to alter consumption without affecting its hedonic impact. Among the principal excitatory afferent pathways, we showed that ventral hippocampal (vHipp) input alone enhances palatability upon low-frequency photostimulation time-locked to consumption. This enhancement in palatability was independent of opioid signaling and not recapitulated by NAcSh or dopamine neuron photostimulation. We further demonstrated that vHipp input photostimulation is sufficient to condition a flavor preference, while its inhibition impedes sucrose-driven flavor preference conditioning.

      Conclusions

      These results demonstrate a novel contribution of vHipp–NAcSh pathway activity to palatability that may relate to its innervation of a particular region or neuronal ensemble in the NAcSh. These findings are consistent with the evidence that vHipp–NAcSh activity is relevant to the pathophysiology of anhedonia and depression as well as the increasing appreciation of hippocampal involvement in people’s food pleasantness ratings, hunger, and weight.

      Keywords

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