Effects of pre-reproductive maternal enrichment on maternal care, offspring’s play behavior and oxytocinergic neurons
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".
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Parental/sensory deprivation or cesarean delivery can lead to disruptions of hypothalamic oxytocin and maternal behavior, while in rats enriched environments increase hypothalamic oxytocin in dams and their male offspring.
“Additionally, parental/sensory deprivation or cesarean delivery can lead to disruptions of hypothalamic OXT and maternal behavior (127-130), while, in rats, enriched environments increase hypothalamic OXT in dams and their male offspring (131).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [131]
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References 105 · Cited by 30
- Authors
- Cutuli, D., Berretta, E., Caporali, P., Sampedro-Piquero, P., De Bartolo, P., Laricchiuta, D., Gelfo, F., Pesoli, M., Foti, F., Farioli Vecchioli, S., & Petrosini, L.
- Affiliations
- Fondazione Santa Lucia (IT)
- Sapienza University of Rome (IT)
- Marconi University (IT)
- Parthenope University of Naples (IT)
- Magna Graecia University (IT)
- Corresponding author
- Cutuli, Debora
- ORCID
- Venue
- Neuropharmacology
- Publisher
- Elsevier BV
- Published
- 2019-02
- Volume
- 145
- Issue
- Pt A
- Pages
- 99-113
- ISSN
- 0028-3908 (ISSN-L)
- OpenAlex
- W2792545625
- Cited by
- 30
- References
- 105
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 4 · 2023: 6 · 2022: 3 · 2021: 4 · 2020: 3 · 2019: 2 · 2018: 3
- FWCI
- 4.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuropharmacology (publishedVersion)
- PubMed (publishedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Funders
- Sapienza Università di Roma
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Keywords
- environmental enrichment, maternal care, pup retrieval, maternal aggression, oxytocinergic neurons, paraventricular nucleus, supraoptic nucleus, transgenerational effects, sex differences, social behavior, intruder aggression
- MeSH terms
- Aggression, Animals, Environment, Female, Housing, Animal, Hypothalamus, Male, Maternal Behavior, Neurons, Oxytocin, Random Allocation, Social Behavior, Time Factors, Rats, Wistar
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