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Chronic hM3Dq-DREADD-mediated chemogenetic activation of parvalbumin-positive inhibitory interneurons in postnatal life alters anxiety and despair-like behavior in adulthood in a task- and sex-dependent manner

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Abstract

Animal models of early adversity or neurodevelopmental disorders are associated with altered parvalbumin (PV)-positive inhibitory interneuron number and function, correlated with a dysregulated excitation–inhibition (E/I) balance that is implicated in the pathophysiology of neuropsychiatric disorders. We sought to address whether altering neuronal activity of PV-positive interneurons during the postnatal developmental window influences the emergence of anxio-depressive behaviors in adulthood, which are known to be perturbed in models of early adversity and neurodevelopmental disorders. We used a PV-Cre::hM3Dq-DREADD bigenic mouse line that selectively expresses the hM3Dq-DREADD receptor in PV-positive interneurons, and chemogenetically enhanced Gq signaling in PV-positive interneurons during the postnatal window via administration of the DREADD agonist, clozapine-N-oxide. Immunofluorescence studies have indicated the selective expression of hM3Dq-DREADD in PV-positive interneurons in limbic circuits, and have revealed a reduction in expression of the neuronal activity marker, c-Fos, in these circuits, following chemogenetic hM3Dq-DREADD-mediated activation of PV-positive inhibitory interneurons. We noted no change in either growth or sensorimotor reflex milestones following chronic hM3Dq-DREADD-mediated chemogenetic activation of PV-positive inhibitory interneurons in postnatal life. Adult male and female PV-Cre::hM3Dq-DREADD bigenic mice with a history of postnatal chemogenetic activation of PV-positive interneurons exhibited a reduction in anxiety and despair-like behavior in adulthood, which was noted in both a behavioral task- and sex-dependent manner. These results indicate that altering neuronal activity within PV-positive interneurons during the critical postnatal developmental window can shape the emergence of anxio-depressive behaviors in adulthood, with sex as a variable playing a key role in determining behavioral outcomes.

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Acknowledgements

We thank Dr. Shital Suryavanshi, and the animal house staff at the Tata Institute of Fundamental Research, Mumbai, for technical assistance. We thank Prof Neeraj Jain, National Brain Research Centre, Manesar, for sharing specific reagents.

Funding

This study was supported by project RTI4003 from the Department of Atomic Energy to Tata Institute of Fundamental Research, and by the Sree Ramakrishna Paramahamsa Research Grant (2020) from the Sree Padmavathi Venkateswara Foundation (SreePVF), Vijayawada, Andhra Pradesh.

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TB and VAV designed the research; TB, SP, and PT performed the research; TB analyzed the data; TB and VAV wrote the paper.

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Correspondence to Vidita A Vaidya.

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Corresponding editor: Aurnab Ghose

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Banerjee, T., Pati, S., Tiwari, P. et al. Chronic hM3Dq-DREADD-mediated chemogenetic activation of parvalbumin-positive inhibitory interneurons in postnatal life alters anxiety and despair-like behavior in adulthood in a task- and sex-dependent manner. J Biosci 47, 68 (2022). https://doi.org/10.1007/s12038-022-00308-0

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