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Social memory deficit caused by dysregulation of the cerebellar vermis

Author

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  • Owen Y. Chao

    (Department of Biomedical Sciences, University of Minnesota Medical School)

  • Salil Saurav Pathak

    (Department of Biomedical Sciences, University of Minnesota Medical School)

  • Hao Zhang

    (Department of Biomedical Sciences, University of Minnesota Medical School)

  • George J. Augustine

    (Nanyang Technological University)

  • Jason M. Christie

    (University of Colorado School of Medicine)

  • Chikako Kikuchi

    (Max Planck Florida Institute for Neuroscience)

  • Hiroki Taniguchi

    (Department of Pathology, Ohio State University Wexner Medical Center
    Chronic Brain Injury, Ohio State University Wexner Medical Center)

  • Yi-Mei Yang

    (Department of Biomedical Sciences, University of Minnesota Medical School
    Department of Neuroscience, University of Minnesota)

Abstract

Social recognition memory (SRM) is a key determinant of social interactions. While the cerebellum emerges as an important region for social behavior, how cerebellar activity affects social functions remains unclear. We selectively increased the excitability of molecular layer interneurons (MLIs) to suppress Purkinje cell firing in the mouse cerebellar vermis. Chemogenetic perturbation of MLIs impaired SRM without affecting sociability, anxiety levels, motor coordination or object recognition. Optogenetic interference of MLIs during distinct phases of a social recognition test revealed the cerebellar engagement in the retrieval, but not encoding, of social information. c-Fos mapping after the social recognition test showed that cerebellar manipulation decreased brain-wide interregional correlations and altered network structure from medial prefrontal cortex and hippocampus-centered to amygdala-centered modules. Anatomical tracing demonstrated hierarchical projections from the central cerebellum to the social brain network integrating amygdalar connections. Our findings suggest that the cerebellum organizes the neural matrix necessary for SRM.

Suggested Citation

  • Owen Y. Chao & Salil Saurav Pathak & Hao Zhang & George J. Augustine & Jason M. Christie & Chikako Kikuchi & Hiroki Taniguchi & Yi-Mei Yang, 2023. "Social memory deficit caused by dysregulation of the cerebellar vermis," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41744-2
    DOI: 10.1038/s41467-023-41744-2
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    References listed on IDEAS

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    1. Ming Ma & Gregory L. Futia & Fabio M. Simoes de Souza & Baris N. Ozbay & Isabel Llano & Emily A. Gibson & Diego Restrepo, 2020. "Molecular layer interneurons in the cerebellum encode for valence in associative learning," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    2. Patricia H. Janak & Kay M. Tye, 2015. "From circuits to behaviour in the amygdala," Nature, Nature, vol. 517(7534), pages 284-292, January.
    3. Ben Deverett & Mikhail Kislin & David W. Tank & Samuel S.-H. Wang, 2019. "Cerebellar disruption impairs working memory during evidence accumulation," Nature Communications, Nature, vol. 10(1), pages 1-7, December.
    4. Frederick L. Hitti & Steven A. Siegelbaum, 2014. "The hippocampal CA2 region is essential for social memory," Nature, Nature, vol. 508(7494), pages 88-92, April.
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