The effects of early social isolation on the motivation for social play in juvenile rats
Abstract
Fifteen-day-old rats were subjected to one of three housing conditions: mother-and-peer (family), peer, and isolation conditions. At 24 days of age, all subjects were rehoused individually. In Experiment 1, play behaviors were monitored in like-raised pairs. Despite their gross lack of social experience, isolation-reared subjects did not exhibit a deficit in frequencies of rough-and-tumble play. It is concluded that the fundamental motivation for rough-and-tumble play is relatively independent of prior learning in rats. Indeed, their elevated dorsal contacts suggested that isolation-raised subjects may have higher appetitive motivation for play. In Experiment 2, the levels of social motivation were compared between family- and isolation-raised animals, using a T-maze. The isolation-raised animals made reliably more choices for social interaction reward over food reward than family-raised animals. Although inconclusive, the results from the two experiments suggest that prolonged social isolation increases the appetitive motivation for social play.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In adolescent rodents, even brief isolation (e.g., 24 h) can cause increased anxiety, hyperactivity, heightened sensitivity to social rewards, and increased seeking of food or drug rewards, making them prone to addictions.
“On a behavioural level, even a brief duration (eg, 24 h) of isolation in adolescent rodents can cause increased anxiety,40 hyperactivity,41 and heightened sensitivity to social rewards,42 which extends to the seeking of food or drug rewards, making these animals particularly prone to developing addictions.43”
From The effects of social deprivation on adolescent development and mental health (2020) · cites this paper as [42]
Social play is a highly rewarding behavior in non-human primates and rats.
“Furthermore, experiments in non-human primates and rats have demonstrated that social play is a highly rewarding behavior (Achterberg et al, 2016;Calcagnetti and Schechter, 1992;Ikemoto and Panksepp, 1992;Normansell and Panksepp, 1990;Trezza et al, 2009).”
From Vasopressin regulates social play behavior in sex-specific ways through glutamate modulation in the lateral septum (2025) · cites this paper as Ikemoto and Panksepp, 1992
Cites
(1977) · Cited by 4,052 · see citing works
Løvtrup, S., & Gould, S. J. (1978) · Systematic Zoology · doi:10.2307/2412825 · Cited by 2,359 · see citing works
Total social isolation in monkeys.
Harlow, H. F., Dodsworth, R. O., & Harlow, M. K. (1965) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.54.1.90 · Cited by 619 · see citing works
The psychobiology of play: Theoretical and methodological perspectives
Panksepp, J., Siviy, S., & Normansell, L. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90005-8 · Cited by 468 · see citing works
Self-citationCritical Periods in Behavioral Development
Scott, J. P. (1962) · Science · doi:10.1126/science.138.3544.949 · Cited by 416 · see citing works
Social deprivation and play in rats
Panksepp, J., & Beatty, W. W. (1980) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(80)91077-8 · Cited by 409 · see citing works
Self-citationUltrasonic vocalization during social interaction and isolation in 2‐week‐old rats
Hofer, M. A., & Shair, H. N. (1978) · Developmental Psychobiology · doi:10.1002/dev.420110513 · Cited by 242 · see citing works
Brief periods of socialization and later behavior in the rat
Einon, D. F., Morgan, M. J., & Kibbler, C. C. (1978) · Developmental Psychobiology · doi:10.1002/dev.420110305 · Cited by 232 · see citing works
Play as a reinforcer for maze-learning in juvenile rats
Humphreys, A. P., & Einon, D. F. (1981) · Animal Behaviour · doi:10.1016/s0003-3472(81)80173-x · Cited by 199 · see citing works
Social play in juvenile rats: A decade of methodological and experimental research
Thor, D. H., & Holloway, W. R. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90004-6 · Cited by 176 · see citing works
Reduction of distress vocalization in chicks by opiate-like peptides
Panksepp, J., Vilberg, T., Bean, N. J., Coy, D. H., & Kastin, A. J. (1978) · Brain Research Bulletin · doi:10.1016/0361-9230(78)90014-x · Cited by 156 · see citing works
Self-citationHofer, M. A., & Shair, H. N. (1987) · Developmental Psychobiology · doi:10.1002/dev.420200410 · Cited by 151 · see citing works
Primus, R. J., & Kellogg, C. K. (1989) · Developmental Psychobiology · doi:10.1002/dev.420220608 · Cited by 146 · see citing works
Comparison of behavioural development in socially isolated and grouped rats
Baenninger, L. P. (1967) · Animal Behaviour · doi:10.1016/0003-3472(67)90018-8 · Cited by 139 · see citing works
Sensory processes in the control of isolation-induced ultrasonic vocalization by 2-week-old rats.
Hofer, M. A., & Shair, H. N. (1980) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077665 · Cited by 131 · see citing works
Gentsch, C., Lichtsteiner, M., Frischknecht, H. R., Feer, H., & Siegfried, B. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90091-1 · Cited by 128 · see citing works
Effects of morphine and naloxone on play‐rewarded spatial discrimination in juvenile rats
Normansell, L., & Panksepp, J. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230108 · Cited by 126 · see citing works
Self-citationDevelopmental analyses of social play behavior in juvenile rats
Thor, D. H., & Holloway, W. R. (1984) · Bulletin of the Psychonomic Society · doi:10.3758/bf03333916 · Cited by 105 · see citing works
Mitchell, G. (1970) · Elsevier eBooks · doi:10.1016/b978-0-12-534001-4.50010-8 · Cited by 99 · see citing works
Gentsch, C., Lichtsteiner, M., Kräuchi, K., & Feer, H. (1982) · Behavioural Brain Research · doi:10.1016/0166-4328(82)90163-2 · Cited by 84 · see citing works
Age at Maternal Separation and Gastric Erosion Susceptibility in the Rat*
Ackerman, S. H., Hofer, M. A., & Weiner, H. (1975) · Psychosomatic Medicine · doi:10.1097/00006842-197503000-00007 · Cited by 74 · see citing works
Brief social isolation, pain responsivity, and morphine analgesia in young rats
Panksepp, J. (1980) · Psychopharmacology · doi:10.1007/bf00433816 · Cited by 68 · see citing works
Self-citationThe organization of sleep and wakefulness after maternal separation in young rats
Hofer, M. A. (1976) · Developmental Psychobiology · doi:10.1002/dev.420090212 · Cited by 68 · see citing works
The Post-Natal Development of Phenotype
(1971) · Archives of Disease in Childhood · doi:10.1136/adc.46.247.402-a · Cited by 58 · see citing works
Early separation of young rats from the mother and the development of play fighting
Janus, K. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90375-1 · Cited by 46 · see citing works
Scopolamine blocks play fighting behavior in juvenile rats.
Thor, D. H., & Holloway, W. (1983) · Physiology and Behavior · doi:10.1016/0031-9384(83)90218-4 · Cited by 41 · see citing works
Psychopharmacology of Social Play
Panksepp, J., Normansell, L., Cox, J. F., Crepeau, L. J., & Sacks, D. S. (1987) · Topics in the neurosciences · doi:10.1007/978-94-009-3359-0_9 · Cited by 36 · see citing works
Self-citationON THE RELATIONSHIP BETWEEN ATTACHMENT AND SEPARATION PROCESSES IN INFANCY
Hofer, M. A. (1983) · Elsevier eBooks · doi:10.1016/b978-0-12-558702-0.50013-3 · Cited by 34 · see citing works
Weaning of Young Rats: Effect of Time on Behavior
Nováková, V. (1966) · Science · doi:10.1126/science.151.3709.475 · Cited by 33 · see citing works
SPEAR, L. P., & Scalzo, F. M. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90258-5 · Cited by 29 · see citing works
Sutton, M. E., & Raskin, L. A. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90541-1 · Cited by 22 · see citing works
Role of the mother during the suckling period of newborn rats on subsequent adult learning
Nováková, V. (1966) · Physiology & Behavior · doi:10.1016/0031-9384(66)90007-2 · Cited by 19 · see citing works
Einon, D. F., & Morgan, M. J. (1978) · Behavioral Biology · doi:10.1016/s0091-6773(78)92763-3 · Cited by 17 · see citing works
Keyser, C. J. (1909) · Science · doi:10.1126/science.30.783.949 · Cited by 4 · see citing works
Medial preoptic area afferents and maternal behavior in the rat
Numan, M. J., McSparren, J., & Numan, M. J. (1988) · The Society for Neuroscience Abstracts · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The effects of social deprivation on adolescent development and mental health
Orben, A., Tomova, L., & Blakemore, S.-J. (2020) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(20)30186-3 · Cited by 1,229 · see citing works
“On a behavioural level, even a brief duration (e.g. 24 hours) of isolation in adolescent rodents can cause increased anxiety( 40 ), hyperactivity( 41 ) and heightened sensitivity to social rewards( 42 ).”
Affective consciousness: core emotional feelings in animals and humans.
Panksepp, J. (2005) · Consciousness and Cognition · doi:10.1016/j.concog.2004.10.004 · Cited by 1,217 · see citing works
Self-citationAutism‐like behavioral phenotypes in BTBR T+tf/J mice
McFarlane, H. G., Kusek, G. K., Yang, M., Phoenix, J. L., Bolivar, V. J., & Crawley, J. N. (2008) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2007.00330.x · Cited by 812 · see citing works
The pleasures of play: pharmacological insights into social reward mechanisms
Trezza, V., Baarendse, P. J. J., & Vanderschuren, L. J. M. J. (2010) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2010.06.008 · Cited by 372 · see citing works
The neurobiology of social play and its rewarding value in rats
Vanderschuren, L. J. M. J., Achterberg, E. J. M., & Trezza, V. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.025 · Cited by 329 · see citing works
Nucleus Accumbens μ-Opioid Receptors Mediate Social Reward
Trezza, V., Damsteegt, R., Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5492-10.2011 · Cited by 263 · 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
Self-citationShultz, S. R., MacFabe, D. F., Ossenkopp, K.-P., Scratch, S., Whelan, J., Taylor, R., & Cain, D. P. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.01.013 · Cited by 217 · see citing works
PANKSEPP, J., NELSON, E., & BEKKEDAL, M. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51914.x · Cited by 210 · see citing works
Self-citationSocial Behavior and Social Motivation in Adolescent Rats
Varlinskaya, E. I., Spear, L. P., & Spear, N. E. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00285-6 · Cited by 194 · see citing works
Endocannabinoids in Amygdala and Nucleus Accumbens Mediate Social Play Reward in Adolescent Rats
Trezza, V., Damsteegt, R., Manduca, A., Petrosino, S., Van Kerkhof, L. W. M., Pasterkamp, R. J., Zhou, Y., Campolongo, P., Cuomo, V., Di Marzo, V., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0114-12.2012 · Cited by 190 · see citing works
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175 · see citing works
Expression of c-fos gene activation during rough and tumble play in juvenile rats
Gordon, N. S., Kollack-Walker, S., Akil, H., & Panksepp, J. (2002) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00762-6 · Cited by 103 · see citing works
Self-citationPeartree, N. A., Hood, L. E., Thiel, K. J., Sanabria, F., Pentkowski, N. S., Chandler, K. N., & Neisewander, J. L. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.10.001 · Cited by 90 · see citing works
Perinatal exposure to polychlorinated biphenyls alters social behaviors in rats
Jolous-Jamshidi, B., Cromwell, H. C., McFarland, A. M., & Meserve, L. A. (2010) · Toxicology Letters · doi:10.1016/j.toxlet.2010.08.015 · Cited by 72 · see citing works
Increased gaze cueing of attention during COVID-19 lockdown.
Dalmaso, M., Castelli, L., & Galfano, G. (2021) · iScience · doi:10.1016/j.isci.2021.103283 · Cited by 31 · 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
“As seen in previous studies of juvenile isolation (Panksepp and Beatty, 1980; Ikemoto and Panksepp, 1992), we found that the ability and motivation to participate in play was not only intact in BARR and ISO animals but was increased relative to our historical data for control-housed animals (Figure 1C; Argue and McCar…”
ResultBredewold, R., Washington, C., & Veenema, A. H. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-024-01987-z · Cited by 13 · see citing works
Orsucci, I. C., Becker, K. D., Ham, J. R., Lee, J. D. A., Bowden, S. M., & Veenema, A. H. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.115080 · Cited by 3 · see citing works
- Authors
- Ikemoto, S., & Panksepp, J.
- Affiliations
- Bowling Green State University (US)
- Corresponding author
- Ikemoto, Satoshi
- ORCID
- Ikemoto, Satoshi
- Venue
- Developmental Psychobiology
- Publisher
- Wiley
- Published
- 1992-05
- Volume
- 25
- Issue
- 4
- Pages
- 261-274
- ISSN
- 0012-1630 (ISSN-L)
- 1098-2302
- OpenAlex
- W2032539293
- Cited by
- 121
- References
- 36
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 4 · 2023: 3 · 2022: 6 · 2021: 7 · 2020: 5 · 2019: 7 · 2018: 4 · 2017: 3 · 2016: 4 · 2015: 7 · 2014: 4 · 2013: 3 · 2012: 3
- FWCI
- 1.37
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Developmental Psychobiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Keywords
- social isolation, social play, rough-and-tumble play, social motivation, appetitive motivation, young rats, social experience, food reward
- MeSH terms
- Animals, Appetitive Behavior, Discrimination Learning, Female, Habituation, Psychophysiologic, Male, Motivation, Motor Activity, Orientation, Play and Playthings, Social Environment, Social Isolation, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
