Isolation during the play period in infancy decreases adult social interactions in rats
Abstract
The effects of 1 or 2 weeks of social isolation immediately after weaning on social activity in adulthood were investigated in rats. In addition, it was studied whether these effects were influenced by social experiences of the cagemate when rehoused after the isolation period. Isolation during weeks 4 and 5 of age caused a reduction of social activity as compared to non-isolated controls. Previous social experiences of the cagemate (isolated or non-isolated) did not affect this decreased social activity. Isolation during week 4 of age resulted in similar effects, but the reduced social activity was not present when the rats were rehoused with non-isolated rats. Isolation during week 5 of age did not influence social activity patterns in adulthood. These findings support the idea of a sensitive period in infancy for subsequent social behavior in rats. It is suggested that especially deprivation of acquiring play behavior underlies the social disturbances in adulthood.
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Animals prevented from playing during the juvenile age exhibit reduced social behavior and inappropriate response to social challenge.
“This idea is supported by play deprivation studies, in which animals prevented from playing during the juvenile age exhibit reduced social behavior and inappropriate response to social challenge (Hol et al., 1999; van den Berg et al., 1999; Von Frijtag et al,. 2002; Stark & Pellis in this Special Issue).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Hol et al., 1999
Social play contributes to the development of adult social and emotional skills.
“Social play contributes to the development of adult social and emotional skills (Pellegrini, 1988; Vanderschuren et al., 1997; Hol et al., 1999; Van den Berg et al., 1999) and is ideal for studying the neurobiology of social development.”
From Sexually dimorphic role for vasopressin in the development of social play (2014) · cites this paper as Hol et al., 1999
Participating in play is essential to appropriate behavior and reproductive success in adulthood.
“While its exact function is debated, various rodent studies on the effects of juvenile social isolation suggest that participating in play is essential to appropriate behavior and reproductive success in adulthood.”
From Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females (2023) · cites this paper as Hol et al., 1999
Juvenile social isolation in rats leads to impairments in social behavior.
“juvenile social isolation in rats leads to impairments in social behavior (Hol et al., 1999; Van den Berg et al., 1999; Von Frijtag et al., 2002)”
From Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females (2023) · cites this paper as Hol et al., 1999
Social isolation from P22-28, but not P29-35, decreases sociability in adulthood in male rats.
“Work from Hol et al. (1999) demonstrated that social isolation from P22–28, but not P29–35, decreases sociability in adulthood in male rats.”
From Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females (2023) · cites this paper as Hol et al. (1999)
Isolation across the full window from P22-35 also decreased sociability.
“Isolation across the full window, from P22–35, also decreased sociability.”
From Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females (2023) · cites this paper as Hol et al. (1999)
These findings on social behaviour are somewhat consistent with previous studies that reported modest reductions in social exploratory behaviour after play deprivation.
“These findings on social behaviour are somewhat consistent with previous studies, that reported modest reductions in social exploratory behaviour after play deprivation (Hol et al. 1999; Van den Berg et al. 1999a, b, c; Lukkes et al. 2009a,b).”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Hol et al. 1999
The postweaning time window is a critical period for PFC maturation and behavioral development.
“consistent with earlier studies that identified this time window as a critical period for PFC maturation and behavioral development”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Hol et al., 1999
Early postweaning social play is important.
“This emphasizes the importance of early postweaning social play”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Hol et al., 1999
Cites
Lore, R., & Flannelly, K. (1977) · Scientific American · doi:10.1038/scientificamerican0577-106 · Cited by 147 · see citing works
Aggressive behaviors in adult rats deprived of playfighting experience as juveniles
Potegal, M., & Einon, D. (1989) · Developmental Psychobiology · doi:10.1002/dev.420220206 · Cited by 133 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
A critical period for social experience-dependent oligodendrocyte maturation and myelination
Makinodan, M., Rosen, K. M., Ito, S., & Corfas, G. (2012) · Science · doi:10.1126/science.1220845 · Cited by 922 · see citing works
The power of play: A pediatric role in enhancing development in young children
Yogman, M., Garner, A., Hutchinson, J., Hirsh-Pasek, K., Golinkoff, R. M., COMMITTEE ON PSYCHOSOCIAL ASPECTS OF CHILD AND FAMILY HEALTH, & COUNCIL ON COMMUNICATIONS AND MEDIA (2018) · Pediatrics · doi:10.1542/peds.2018-2058 · Cited by 758 · see citing works
Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2004) · Developmental Psychobiology · doi:10.1002/dev.20025 · Cited by 389 · see citing works
Silva-Gómez, A. B., Rojas, D., Juárez, I., & Flores, G. (2003) · Brain Research · doi:10.1016/s0006-8993(03)03042-7 · Cited by 336 · see citing works
Social reward among juvenile mice
Panksepp, J. B., & Lahvis, G. P. (2007) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2006.00295.x · Cited by 248 · see citing works
Burke, A. R., McCormick, C. M., Pellis, S. M., & Lukkes, J. L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.018 · Cited by 225 · see citing works
Bell, H. C., Pellis, S. M., & Kolb, B. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.09.029 · Cited by 217 · see citing works
Vanderschuren, L. J. M. J., & Trezza, V. (2013) · Current Topics in Behavioral Neurosciences · doi:10.1007/978-3-662-45758-0_268 · Cited by 200 · see citing works
Isolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats
Van den Berg, C. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00099-6 · Cited by 165 · see citing works
Bidirectional cannabinoid modulation of social behavior in adolescent rats
Trezza, V., & Vanderschuren, L. J. M. J. (2008) · Psychopharmacology · doi:10.1007/s00213-007-1025-3 · Cited by 159 · see citing works
Preference for social contact versus environmental enrichment in male laboratory mice
Van Loo, P. L. P., Van de Weerd, H. A., Van Zutphen, L. F. M., & Baumans, V. (2004) · Laboratory Animals · doi:10.1258/002367704322968867 · Cited by 118 · see citing works
Von Frijtag, J. C., Schot, M., van den Bos, R., & Spruijt, B. M. (2002) · Developmental Psychobiology · doi:10.1002/dev.10057 · Cited by 116 · see citing works
Self-citationHermes, G., Li, N., Duman, C., & Duman, R. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.12.019 · Cited by 111 · see citing works
Lord, K. (2013) · Ethology · doi:10.1111/eth.12044 · Cited by 100 · see citing works
Burleson, C. A., Pedersen, R. W., Seddighi, S., DeBusk, L. E., Burghardt, G. M., & Cooper, M. A. (2016) · Behavioral Neuroscience · doi:10.1037/bne0000148 · Cited by 69 · see citing works
Bijlsma, A., Omrani, A., Spoelder, M., Verharen, J. P. H., Bauer, L., Cornelis, C., de Zwart, B., van Dorland, R., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.0524-22.2022 · Cited by 54 · see citing works
Sexually dimorphic role for vasopressin in the development of social play
Paul, M. J., Terranova, J. I., Probst, C. K., Murray, E. K., Ismail, N. I., & de Vries, G. J. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00058 · Cited by 51 · see citing works
“Social play contributes to the development of adult social and emotional skills (Pellegrini, 1988; Vanderschuren et al., 1997; Hol et al., 1999; Van den Berg et al., 1999) and is ideal for studying the neurobiology of social development.”
BackgroundInfluentialDevelopmental origins of sex differences in the neural circuitry of play
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1723370 · Cited by 34 · see citing works
Marquardt, A. E., VanRyzin, J. W., Fuquen, R. W., & McCarthy, M. M. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1076765 · Cited by 31 · see citing works
“Various studies have found that juvenile social isolation in rats leads to impairments in social behavior (Hol et al., 1999; Van den Berg et al., 1999; Von Frijtag et al., 2002), cognition (Einon et al.”
BackgroundColonnello, V., Iacobucci, P., Anderson, M. P., & Panksepp, J. (2011) · Developmental Psychobiology · doi:10.1002/dev.20520 · Cited by 13 · see citing works
Bredewold, R., Washington, C., & Veenema, A. H. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-024-01987-z · Cited by 13 · see citing works
Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia
Achterberg, E. J. M., Biemans, B., & Vanderschuren, L. J. M. J. (2025) · Psychopharmacology · doi:10.1007/s00213-024-06559-z · Cited by 9 · see citing works
“These findings on social behaviour are somewhat consistent with previous studies, that reported modest reductions in social exploratory behaviour after play deprivation (Hol et al. 1999; Van den Berg et al. 1999a, b, c; Lukkes et al. 2009a,b).”
Longitudinal study of the spectral composition of behavioral rhythms in the rat
Castro, E. C. V., & Andrade, M. M. M. (2005) · Biological Rhythm Research · doi:10.1080/09291010400028880 · Cited by 5 · see citing works
- Authors
- Hol, T., Van den Berg, C. L., Van Ree, J. M., & Spruijt, B. M.
- Affiliations
- Utrecht University (NL)
- Corresponding author
- Spruijt, B.M.
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 1999-04
- Volume
- 100
- Issue
- 1-2
- Pages
- 91-97
- ISSN
- 0166-4328 (ISSN-L)
- OpenAlex
- W2026587663
- Cited by
- 212
- References
- 2
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 10 · 2023: 10 · 2022: 3 · 2021: 10 · 2020: 5 · 2019: 11 · 2018: 14 · 2017: 10 · 2016: 11 · 2015: 11 · 2014: 13 · 2013: 8 · 2012: 9
- FWCI
- 8.43
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Keywords
- social isolation, infancy, sensitive period, social behavior, play behavior, rehousing
- MeSH terms
- Age Factors, Animals, Male, Play and Playthings, Psychosocial Deprivation, Social Behavior, Social Isolation, Weaning, Rats, Wistar, Rats
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