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Activation patterns in male and female forebrain circuitries during food consumption under novelty

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Abstract

The influence of novelty on feeding behavior is significant and can override both homeostatic and hedonic drives due to the uncertainty of potential danger. Previous work found that novel food hypophagia is enhanced in a novel environment and that males habituate faster than females. The current study’s aim was to identify the neural substrates of separate effects of food and context novelty. Adult male and female rats were tested for consumption of a novel or familiar food in either a familiar or in a novel context. Test-induced Fos expression was measured in the amygdalar, thalamic, striatal, and prefrontal cortex regions that are important for appetitive responding, contextual processing, and reward motivation. Food and context novelty induced strikingly different activation patterns. Novel context induced Fos robustly in almost every region analyzed, including the central (CEA) and basolateral complex nuclei of the amygdala, the thalamic paraventricular (PVT) and reuniens nuclei, the nucleus accumbens (ACB), the medial prefrontal cortex prelimbic and infralimbic areas, and the dorsal agranular insular cortex (AI). Novel food induced Fos in a few select regions: the CEA, anterior basomedial nucleus of the amygdala, anterior PVT, and posterior AI. There were also sex differences in activation patterns. The capsular and lateral CEA had greater activation for male groups and the anterior PVT, ACB ventral core and shell had greater activation for female groups. These activation patterns and correlations between regions, suggest that distinct functional circuitries control feeding behavior when food is novel and when eating occurs in a novel environment.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We acknowledge Laura Buczek, William Parsons, Kate Gershfeld, and Nadia Moumine, for technical support and assistance. A portion of the research reported here partially fulfilled the requirements for the Senior Honors Theses awarded to MW and SJM and for the degree of PhD awarded to EMG by Boston College.

Funding

This work was supported by the National Institutes of Health, NIDDK grant R01DK085721 to GDP.

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Contributions

GDP conceptualized the study and supervised the experiment and directed the data analysis. EMG and GDP designed the experiments. EMG carried out the experiment. EMG, SJM, and MEW conducted histological preparation and analysis. EMG, SJM, and MEW prepared figures. EMG and GDP wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Gorica D. Petrovich.

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The authors have no relevant financial or non-financial interests to disclose.

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All housing and testing procedures were in compliance with the National Institutes of Health Guidelines for Care and Use of Laboratory Animals and approved by the Boston College Institutional Animal Care and Use Committee.

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Greiner, E.M., Witt, M.E., Moran, S.J. et al. Activation patterns in male and female forebrain circuitries during food consumption under novelty. Brain Struct Funct 229, 403–429 (2024). https://doi.org/10.1007/s00429-023-02742-8

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  • DOI: https://doi.org/10.1007/s00429-023-02742-8

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