Early social experience is critical for the development of cognitive control and dopamine modulation of prefrontal cortex function
Open accessAbstract
Social experiences during youth are thought to be critical for proper social and cognitive development. Conversely, social insults during development can cause long-lasting behavioral impairments and increase the vulnerability for psychopathology later in life. To investigate the importance of social experience during the juvenile and early adolescent stage for the development of cognitive control capacities, rats were socially isolated from postnatal day 21 to 42 followed by re-socialization until they reached adulthood. Subsequently, two behavioral dimensions of impulsivity (impulsive action in the five-choice serial reaction time task (5-CSRTT) and impulsive choice in the delayed reward task) and decision making (in the rat gambling task) were assessed. In a separate group of animals, long-lasting cellular and synaptic changes in adult medial prefrontal cortex (PFC) pyramidal neurons were determined following social isolation. Juvenile and early adolescent social isolation resulted in impairments in impulsive action and decision making under novel or challenging circumstances. Moreover, socially isolated rats had a reduced response to enhancement of dopaminergic neurotransmission (using amphetamine or GBR12909) in the 5-CSRTT under challenging conditions. Impulsive choice was not affected by social isolation. These behavioral deficits were accompanied by a loss of sensitivity to dopamine of pyramidal neurons in the medial PFC. Our data show long-lasting deleterious effects of early social isolation on cognitive control and its neural substrates. Alterations in prefrontal cognitive control mechanisms may contribute to the enhanced risk for psychiatric disorders induced by aberrations in the early social environment.
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Functional studies in adult rodent models link genetic or experimentally induced alterations in DA neuron activity, DA release, and receptor binding to transdiagnostic changes in motivation and cognitive control.
“Functional studies in adult rodent models have linked genetic or experimentally induced alterations in DA neuron activity, DA release, and receptor binding to transdiagnostic changes in motivation and cognitive control [49, 132–135].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [135]
The Discussion reports that social isolation during early development impaired adult rats’ impulse control and decision making and reduced dopamine modulation of prefrontal synaptic responses. It does not establish genetic alterations, measured changes in dopamine-neuron activity, dopamine release or receptor binding, or transdiagnostic changes in motivation; it also leaves the causal link between dopamine sensitivity and the behavioral deficits unresolved. The indexed passages provide no page numbers. (LLM, conf=0.85)
Experimental — accuracy not yet measuredRats demonstrate enhanced cognitive abilities and a rich social repertoire paired with neural complexity, particularly in brain regions implicated in ASD pathology such as the frontal cortex.
“Rats demonstrate enhanced cognitive abilities and a rich social repertoire paired with neural complexity, particularly in brain regions implicated in ASD pathology such as the frontal cortex [10–12].”
From Behavioral Phenotyping of Juvenile Long-Evans and Sprague-Dawley Rats: Implications for Preclinical Models of Autism Spectrum Disorders (2016) · cites this paper as [12]
The Introduction (page unavailable) describes increasingly complex social behavior and abundant social play in juvenile rodents. The Discussion (page unavailable) links social experience to cognitive capacities and prefrontal cortex function in rats. The paper does not establish that rats have enhanced cognitive abilities or neural complexity, or identify the frontal cortex as a region implicated in ASD pathology. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe development of the medial prefrontal cortex and associated socio-cognitive skills is influenced by the experience of rough-and-tumble play with peers in the juvenile period (about 28-40 days post birth).
“the development of the medial prefrontal cortex (mPFC) and associated socio-cognitive skills is influenced by the experience of RTP with peers in the juvenile period (about 28–40 days post birth; Bell et al., 2010; Baarendse et al., 2013; Schneider et al., 2016)”
From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Baarendse et al., 2013
The Introduction and Discussion link juvenile social experience to prefrontal development and cognitive control, and report altered mPFC dopamine sensitivity after social isolation in rats. But the study isolated rats during postnatal days 21–42; it did not isolate the effects of rough-and-tumble play or establish the narrower 28–40-day window. No page numbers are provided in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredDeprivation of social play leads to long-lasting impairments in the social, emotional and cognitive domain.
“previous studies have shown that deprivation of social play leads to long-lasting impairments in the social, emotional and cognitive domain (Baarendse et al. 2013; Bijlsma et al. 2022; Lukkes et al. 2009a; Potegal and Einon 1989; Van den Berg et al. 1999a; Whitaker et al. 2013, for reviews see Vanderschuren and Trezza 2014; Pellis et al. 2023).”
From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Baarendse et al. 2013
The Discussion reports that social-contact deprivation in post-weaning rats produced social deficits lasting into adulthood, and that this study found adult cognitive-control deficits after juvenile social isolation. The paper studied social isolation rather than selective deprivation of play, and the cited passages do not establish long-lasting emotional impairments. (LLM, conf=0.86)
Experimental — accuracy not yet measuredJuvenile social isolation in rats leads to impairments in cognition.
“cognition (Einon et al., 1978; Baarendse et al., 2013; Yusufishaq and Rosenkranz, 2013)”
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 Baarendse et al., 2013
During adolescence, social and cognitive skills depend on peer-to-peer interactions.
“During adolescence, social and cognitive skills depend on peer-to-peer interactions (Vanderschuren et al., 1997; Baarendse et al., 2013), and acute social isolation in rodents is sufficient to cause behavioral abnormalities, including increased vulnerability to drug addiction and depressive-like behavior, later in life (Lampert et al., 2017; Takatsu-Coleman et al., 2013; Whitaker et al., 2013).”
From Oxytocin neurons mediate the effect of social isolation via the VTA circuits (2022) · cites this paper as Baarendse et al., 2013
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- Authors
- Baarendse, P. J. J., Counotte, D. S., O'Donnell, P., & Vanderschuren, L. J. M. J.
- Affiliations
- University Medical Center Utrecht (NL)
- University of Maryland, Baltimore (US)
- Utrecht University (NL)
- Corresponding author
- Vanderschuren, Louk J M J
- Venue
- Neuropsychopharmacology
- Published
- 2013-02-12
- Volume
- 38
- Issue
- 8
- Pages
- 1485-1494
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC3682143
- OpenAlex
- W2071038788
- Cited by
- 206
- References
- 9
- Citations by year
- 2026: 8 · 2025: 15 · 2024: 15 · 2023: 23 · 2022: 14 · 2021: 12 · 2020: 18 · 2019: 8 · 2018: 15 · 2017: 18 · 2016: 22 · 2015: 18 · 2014: 9 · 2013: 11
- FWCI
- 9.80
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Funders
- National Institute on Drug Abuse (R01DA014020, R01DA022628)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Keywords
- social isolation, cognitive control, dopaminergic modulation, medial prefrontal cortex, impulsivity, decision-making, adolescent development, pyramidal neurons, synaptic plasticity, amphetamine sensitivity, GBR 12909, 5-choice serial reaction time task, gambling task, psychiatric vulnerability
- MeSH terms
- Age Factors, Animals, Cognition, Dopamine, Impulsive Behavior, Male, Reaction Time, Social Environment, Social Isolation, Prefrontal Cortex, Rats, Long-Evans, Rats
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