Cited by 258Neurotransmitter Receptor Influence on BehaviorNeuroendocrine regulation and behaviorPrimate Behavior and Ecology

Evaluating the rewarding nature of social interactions in laboratory animals

Open access
Trezza, Viviana, Campolongo, Patrizia, Vanderschuren, Louk J.M.J.·2011·Developmental Cognitive Neuroscience

Abstract

Positive social interactions are essential for emotional well-being, healthy development, establishment and maintenance of adequate social structures and reproductive success of humans and animals. Here, we review the studies that have investigated whether forms of social interaction that occur in different phases of the lifespan of animals, i.e., maternal behavior, social play and sexual interaction are rewarding in rodents and non-human primates. We show that these three forms of social interaction can be used as incentive for place conditioning, lever pressing and maze learning, three setups that have been extensively used to study the rewarding properties of food and drugs of abuse and their neural underpinnings. The experience of positive social interactions during key developmental ages has profound and long-lasting effects on brain function and behavior in emotional, motivational and cognitive domains. For instance, pup interaction is more rewarding than cocaine for early postpartum dams and rats deprived of the opportunity to play during adolescence show social and cognitive impairments at adulthood. Furthermore, sexual behavior is only overtly rewarding when animals can control the rate at which the sexual interaction occurs. Last, we discuss how animal models contributed to our understanding of social reward mechanisms and its psychological components throughout development.

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Crossref · 10.1016/j.dcn.2011.05.007

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  • Play is a behavior common in many young mammalian species, including human children, juvenile monkeys and rats.

    “Given that play is a behavior common in many young mammalian species, including human children, juvenile monkeys and rats, we focused our efforts on quantification of play behaviors [53–55].”

    From Behavioral Phenotyping of Juvenile Long-Evans and Sprague-Dawley Rats: Implications for Preclinical Models of Autism Spectrum Disorders (2016) · cites this paper as [53]

    Section 2.2 describes social play as characteristic of young mammals and discusses adolescent rats. Section 3.2 also reports play in young chimpanzees, supporting the primate example. Our copy does not specifically address play in human children, so that example is not verified by this source. (LLM, conf=0.82)

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  • The rewarding properties of social play behaviour in rats have been well-documented in place conditioning and operant conditioning setups.

    “The rewarding properties of social play behaviour in rats have been well-documented in place conditioning and operant conditioning setups (Calcagnetti and Schechter 1992; Trezza et al. 2011; Achterberg et al. 2016a,b, 2019).”

    From Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia (2025) · cites this paper as Trezza et al. 2011

    Section 2.2 reports consistent evidence from place-conditioning studies that social play is rewarding in adolescent rats. The paper also describes operant responding for play in section 3.2, but the lever-pressing example retrieved there concerns chimpanzees; its rat play-reinforcement examples in section 4.2 use a T-maze. It therefore does not fully substantiate the claim about operant conditioning setups in rats. (LLM, conf=0.83)

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Cites

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Research works printed but not linked: 6

  1. Lee, A., Clancy, S., Fleming, A.S., 1999. Mother rats bar-press for pups: effects of lesions of the mpoa and limbic sites on maternal behavior and operant responding for pup-reinforcement. Behav. Brain Res. 100, 15-31.
  2. Pellis, S.M., Pellis, V., 2009. The Playful Brain: Venturing to the Limits of Neuroscience. Oneworld Publications, Oxford, UK.
  3. Pfaus, J.G., Kippin, T.E., Centeno, S., 2001. Conditioning and sexual behav- ior: a review. Horm. Behav. 40, 291-321.
  4. Tzschentke, T.M., 1998. Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog. Neurobiol. 56, 613-672.
  5. Wenk, G.L., 2001. Assessment of spatial memory using the T maze. Curr. Protoc. Neurosci. (Chapter 8, Unit 8 5B).
  6. Wilsoncroft, W.E., 1969. Babies by bar-press: maternal behavior in the rat. Behav. Res. Methods 1, 229-230.

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Authors
Trezza, V., Campolongo, P., & Vanderschuren, L. J. M. J.
Affiliations
  • Roma Tre University (IT)
  • Sapienza University of Rome (IT)
  • Utrecht University (NL)
Corresponding author
  • Trezza, Viviana
  • Vanderschuren, Louk J.M.J.
Venue
Developmental Cognitive Neuroscience
Publisher
Elsevier BV
Published
2011-10
Volume
1
Issue
4
Pages
444-458
ISSN
1878-9293 (ISSN-L)
OpenAlex
W1980926695
Cited by
258
References
11
Citations by year
2026: 11 · 2025: 16 · 2024: 19 · 2023: 24 · 2022: 23 · 2021: 20 · 2020: 19 · 2019: 19 · 2018: 25 · 2017: 12 · 2016: 21 · 2015: 18 · 2014: 11 · 2013: 12 · 2012: 7
FWCI
3.98
Type
journal article
Language
en
Open access
Locations
  • Developmental Cognitive Neuroscience (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
  • IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
  • Iris (Roma Tre University) (submittedVersion)
Funders
  • National Institute on Drug Abuse (R01 DA022628-01)
  • Dutch Top Institute Pharma
  • Veni (91611052)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
Keywords
social reward, social interaction, maternal behavior, social play, sexual interaction, place conditioning, lever pressing, maze learning, cocaine reward, non-human primates, rodents, developmental effects, emotional well-being, motivation, cognitive impairment
MeSH terms
Animals, Animals, Laboratory, Humans, Interpersonal Relations, Maternal Behavior, Reward, Sexual Behavior, Social Behavior, Rats

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