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Environmental Enrichment Differentially Activates Neural Circuits in FVB/N Mice, Inducing Social Interaction in Females but Agonistic Behavior in Males

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Abstract

Environmental enrichment induces behavioral and structural modifications in rodents and influences the capability of mice to cope with stress. However, little is understood about hippocampal neurogenesis and the appearance of social/agonistic (aggressive) behavior upon activation of different neuronal circuits in FVB/N mice. Thus, in this study we hypothesized that environmental enrichment differentially regulates neurogenesis, neural circuit activation and social/agonistic behavior in male and female FVB/N mice. We explored the (1) neurogenic process as an indicative of neuroplasticity, (2) neuronal activation in the limbic system, and (3) social behavior using the resident-intruder test. On postnatal day 23 (PD23), mice were assigned to one of two groups: Standard Housing or Environmental Enrichment. At PD53, rodents underwent the resident-intruder test to evaluate social behaviors. Results revealed that environmental enrichment increased neurogenesis and social interaction in females. In males, environmental enrichment increased neurogenesis and agonistic behavior. Enriched male mice expressed higher levels of agonistic-related behavior than female mice housed under the same conditions. Neural circuit analysis showed lower activation in the amygdala of enriched males and higher activation in enriched females than their respective controls. Enriched females also showed higher activation in the frontal cortex without differences in male groups. Moreover, the insular cortex was less activated in females than in males. Thus, our results indicate that environmental enrichment has different effects on neuroplasticity and social/agonistic behavior in FVB/N mice, suggesting the relevance of sexual dimorphism in response to environmental stimuli.

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Data Availability

The relevant data are within the manuscript. However, the datasets analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We thank Diana Laura Acacio-Martínez and Mario Castro-García for technical assistance and support for software handling. We also thank Liliana Soto Gutiérrez for administrative procedures. We thank Dr. Martha León-Olea for allowing us to use the confocal microscopy facilities of the Instituto Nacional de Psiquiatría Ramón de la Fuente Muñiz. The authors thank LCC. Jessica G. Norris for proofreading the English version of this manuscript.

Funding

This research was funded by INPRFM grant number 2000 to GBRR. Some of the equipment used in the present study was kindly financed by CONACYT (Grant Infraestructura 2015; 254773 to GBRR). S.O.H. was supported by INPRF-Programa Igualdad entre hombres y mujeres y Coordinado por INMujeres, SHCP y Cámara de Diputados, LXII.

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Authors and Affiliations

  1. Laboratorio of Neurogénesis, Subdirección de Investigaciones Clínicas, Instituto Nacional de Psiquiatría “Ramón de La Fuente Muñiz”, Calzada México-Xochimilco No. 101, Colonia San Lorenzo Huipulco, Delegación Tlalpan, C.P. 14370, México City, México

    Edith Araceli Cabrera-Muñoz, Sandra Olvera-Hernández, David Meneses-San Juan, Leonardo Ortiz-López & Gerardo Bernabé Ramírez Rodríguez

  2. Laboratorio of Neuropsicofarmacología, Dirección de Neurociencias, Instituto Nacional de Psiquiatría “Ramón de La Fuente Muñiz”, Calzada México-Xochimilco 101, C.P. 14370, México City, México

    Nelly Maritza Vega-Rivera

  3. Departamento de Neurobiología Celular y Molecular, Instituto de Neurobiología. Universidad Nacional Autónoma de México, Campus Juriquilla. Boulevard Juriquilla 3001, C.P. 76230, Juriquilla, Querétaro, México

    Daniel Reyes-Haro

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Contributions

Conceptualization, GBR-R, SOH, and NMV-R; methodology, EACM, and SOH; formal analysis, DMS-J; investigation, EACM, and SOH; resources, GBR-R, and DR-H; data curation, EACM, and DMS-J; methodology (confocal micrsocopy images), LO-L; writing—original draft preparation, EACM; writing—review and editing, GBR-R, and NMV-R; visualization, GBR-R; supervision, GBR-R; project administration, GBR-R; funding acquisition, GBR-R. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Gerardo Bernabé Ramírez Rodríguez.

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All institutional and legal regulations regarding animal ethics, care, and handling were performed following the Mexican Official Standard for animal care (NOM-062-ZOO-1999) and approved by the local Institutional Ethics Committee of the National Institute of Psychiatry “Ramón de la Fuente Muñiz” (IACUC: CEI/C/009/2013).

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Cabrera-Muñoz, E.A., Olvera-Hernández, S., Vega-Rivera, N.M. et al. Environmental Enrichment Differentially Activates Neural Circuits in FVB/N Mice, Inducing Social Interaction in Females but Agonistic Behavior in Males. Neurochem Res 47, 781–794 (2022). https://doi.org/10.1007/s11064-021-03487-8

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