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Attenuation of social preference and alteration of cortical neurons following adolescent cerebellar nuclei perturbation

Molecular Psychiatry (2025)Cite this article

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Abstract

Connections between one of the main outputs of the cerebellar cortex, the lateral cerebellar nuclei (LCN), to reward-related circuits may explain social deficits resulting from cerebellar critical period perturbations. To examine the influence of LCN development on social behavior, local neural activity was manipulated in mice using Designer Receptors Exclusively Activated by Designer Drugs (DREADDs) from postnatal day 21–35. Adolescent social behavior was assessed using a three-chamber assay. Results revealed the LCN perturbation abolished male social preference. LCN manipulated mice were found to have less neural activation (cFos) in the ventral tegmental area, nucleus accumbens, and anterior cingulate cortex (ACC). Additionally, mice that received the excitatory DREADD perturbation showed increased dendritic complexity in the ACC. These results suggest a chronic perturbation in the LCN during juvenile and early adolescent development impacts social behavior and results in changes to cortical activity and structure observed in adolescence.

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Fig. 1: Experimental timeline, chemogenetic approach, and three-chamber task.
Fig. 2: Sex-differences in social behavior.
Fig. 3: VTA cFos correlations with social behavior.
Fig. 4: cFos expression in the nucleus accumbens.
Fig. 5: Changes in ACC activity and dendritic complexity.
Fig. 6: Sex-differences in pyramidal neuron spines.
Fig. 7: Behavioral correlates with neural mechanisms.

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Data availability

The dataset is available at Arizona State University dataverse: https://doi.org/10.48349/ASU/4MT3XU and https://github.com/verpeutlab/Dentatesocial

Code availability

All experimental and analysis code is available at Arizona State University dataverse: https://doi.org/10.48349/ASU/4MT3XU and https://github.com/verpeutlab/Dentatesocial

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Acknowledgements

This work was supported by: the Institute for Mental Health Research, Institute for Social Science Research, Nancy Eisenberg Junior Faculty scholar Award, Arizona Department of Health Sciences (ADHS14-052688), US Department of Health and Human Services and the state of Arizona (ADHS Grant No. CTR057001), National Institute on Aging (NIA) of the National Institutes of Health (NIH) (P30AG019610), Arizona Alzheimer’s Disease Research Center REC Fellows Program and Arizona Alzheimer’s Consortium. Figures were created with Biorender.com. We would like to thank Samantha Bowser for animal colony management, Federico Sanabria for statistical analysis discussions, and Mikhail Kislin for assistance with calcium signaling analysis.

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  1. Arizona State University, Department of Psychology, Tempe, AZ, 85287, USA

    Tristan T. Lyle, Kristin Masho Elbeh, Daniel Chambers, Henrique Vieira & Jessica L. Verpeut

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  1. Tristan T. Lyle
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Contributions

Tristan Lyle: Conceptualization, data analysis and curation, validation, investigation, visualization, methodology, writing, and project administration. Kristin Masho Elbeh: Data analysis, curation, and writing. Daniel Chambers: Data analysis and curation. Henrique Vierira: Data analysis and curation. Jessica L Verpeut: Conceptualization, data analysis and curation, funding acquisition, validation, investigation, visualization, methodology, writing, and project administration.

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Correspondence to Tristan T. Lyle or Jessica L. Verpeut.

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All study protocols and methods were approved by the Institutional Animal Care and Use Committee at Arizona State University (protocol #24-2052 R) in accordance with guidelines from the National Institutes of Health Guide for the Care and Use of Laboratory Animals.

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Lyle, T.T., Masho Elbeh, K., Chambers, D. et al. Attenuation of social preference and alteration of cortical neurons following adolescent cerebellar nuclei perturbation. Mol Psychiatry (2025). https://doi.org/10.1038/s41380-025-03404-3

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