Effects of pre-reproductive maternal enrichment on maternal care, offspring's play behavior and oxytocinergic neurons

Debora Cutuli; Erica Berretta; Paola Caporali; Patricia Sampedro-Piquero; Paola De Bartolo; Daniela Laricchiuta; Francesca Gelfo; Matteo Pesoli; Francesca Foti; Stefano Farioli Vecchioli; Laura Petrosini

doi:10.1016/j.neuropharm.2018.02.015

Effects of pre-reproductive maternal enrichment on maternal care, offspring's play behavior and oxytocinergic neurons

Neuropharmacology. 2019 Feb;145(Pt A):99-113. doi: 10.1016/j.neuropharm.2018.02.015. Epub 2018 Feb 17.

Affiliations

¹ Department of Psychology, Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy; Fondazione Santa Lucia, Rome, Italy. Electronic address: debora.cutuli@uniroma1.it.
² Department of Psychology, Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy; Fondazione Santa Lucia, Rome, Italy.
³ Department of Psychology, Faculty of Medicine and Psychology, Sapienza University of Rome, Rome, Italy.
⁴ Departamento de Psicobiología y Metodología de las Ciencias del Comportamiento. Facultad de Psicología, Instituto de Investigación Biomédica de Málaga (IBIMA), Universidad de Málaga, Spain.
⁵ Fondazione Santa Lucia, Rome, Italy; Department of TeCoS, Guglielmo Marconi University, Rome, Italy.
⁶ Fondazione Santa Lucia, Rome, Italy; Department of Motor Science and Wellness, University Parthenope, Naples, Italy.
⁷ Fondazione Santa Lucia, Rome, Italy; Department of Medical and Surgical Sciences, Magna Graecia University of Catanzaro, Catanzaro, Italy.
⁸ Institute of Cell Biology and Neurobiology, National Research Council, Rome, Italy.

PMID: 29462694
DOI: 10.1016/j.neuropharm.2018.02.015

Abstract

Potentiating social, cognitive, and sensorimotor stimulations the Environmental Enrichment (EE) increases levels of novelty and complexity experienced by individuals. Growing evidence demonstrates that parental EE experience, even occurring in the pre-reproductive phase, affects behavioral and neural developmental trajectories of the offspring. To discover how the accumulation of early maternal complex experiences may inform and shape the social behavior of the following generation, we examined the effects of pre-reproductive enrichment of dams (post-natal days 21-72) on the play performances of their male and female adolescent offspring. Furthermore, we examined the effects of pre-reproductive enrichment on maternal behavior (during post-partum days 1-10) and male intruder aggression (on post-partum day 11). Since oxytocin modulates maternal care, social bonding, and agonistic behavior, the number of oxytocinergic neurons of the paraventricular (PVN) and supraoptic (SON) nuclei was examined in both dams and offspring. Results revealed that enriched females exhibited higher levels of pup-oriented behaviors, especially Crouching, and initiated pup-retrieval more quickly than standard females after the maternal aggression test. Such behavioral peculiarities were accompanied by increased levels of oxytocinergic neurons in PVN and SON. Moreover, pre-reproductive maternal EE cross-generationally influenced the offspring according to sex. Indeed, male pups born to enriched females exhibited a reduced play fighting associated with a higher number of oxytocinergic neurons in SON in comparison to male pups born to standard-housed females. In conclusion, pre-reproductive EE to the mothers affects their maternal care and has a cross-generational impact on the social behavior of their offspring that do not directly experiences EE. This article is part of the Special Issue entitled "Neurobiology of Environmental Enrichment".

Keywords: Adolescence; Environmental enrichment; Maternal care and aggression; Oxytocin; Rats; Social play.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Aggression
Animals
Environment*
Female
Housing, Animal
Hypothalamus / cytology
Hypothalamus / metabolism
Male
Maternal Behavior / physiology
Maternal Behavior / psychology
Neurons / cytology
Neurons / metabolism*
Oxytocin / metabolism*
Random Allocation
Rats, Wistar
Social Behavior*
Time Factors

Substances

Oxytocin