The DOI matches its Crossref record; 36 of the 36 references it cites were found in a registry or an index.
Expression of c-fos gene activation during rough and tumble play in juvenile rats
Abstract
Rough and tumble (R&T) play is an intrinsic behavior in most mammals. However, unlike sex and aggression, play has not been well characterized in terms of neuronal circuitry. We employed in situ hybridization to explore the differences of c-fos mRNA activation in juvenile rats that had been allowed R&T play for a total of 30 min before sacrifice contrasted to animals with comparable histories that had received no play. Densitometric estimates of c-fos gene activation revealed that the deep and dorsolateral tectum, inferior colliculus, dorsal periaquaductal gray, ventromedial hypothalamus, dorsal and ventral striatum, and somatosensory cortex were significantly more activated in animals that had played than those that had not. Prior play dominance and amount of social experience had no clear effects on the levels of c-fos gene expression. This provides a variety of new hypotheses concerning the role of various brain areas in the elaboration of R&T play behavior, but the important role of other types of motor arousal in the differential effects were not evaluated in this study.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
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 the citing paper
“The activation patterns in many of these regions correlated with one another, suggesting that the coordinated activity, rather than individual activation, of specific brain circuits is necessary for proper play behavior.”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Gordon et al., 2002
In the citing paper
“Using this methodology, two leading play research groups demonstrated that play activates several distinct brain regions, including those involved in motivation, reward, sensory, and motor processing (Gordon et al., 2002; van Kerkhof et al., 2014).”
From Developmental origins of sex differences in the neural circuitry of play (2020) · cites this paper as Gordon et al., 2002
In the citing paper
“Social play enhances neuronal activity in a broad network of limbic and corticostriatal structures”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Gordon et al., 2002
Citations
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585
Affective Neuroscience: The Foundations of Human and Animal Emotions
Panksepp, J. (1998) · doi:10.1093/oso/9780195096736.001.0001 · Cited by 4,428
Self-citationIkemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450
Self-citationThe neurobiology of social play behavior in rats
Vanderschuren, L. J. M. J., Niesink, R. J. M., & Van Pee, J. M. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00020-6 · Cited by 559
Panksepp, J. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140405 · Cited by 537
Self-citationThe 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
Self-citationAnticipation of play elicits high-frequency ultrasonic vocalizations in young rats.
Knutson, B. D., Burgdorf, J. S., & Panksepp, J. (1998) · Journal of comparative psychology · doi:10.1037/0735-7036.112.1.65 · Cited by 456
Self-citation(1998) · Journal of Consciousness Studies · Cited by 332
Self-citationKollack‐Walker, S., & Newman, S. W. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00563-k · Cited by 315
Self-citationPlace conditioning reveals the rewarding aspect of social interaction in juvenile rats
Calcagnetti, D. J., & Schechter, M. D. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90101-7 · Cited by 284
Neurochemical mechanisms of the defensive behavior in the dorsal midbrain
Brandão, M. L., Anseloni, V. Z., Pandóssio, J. E., De Araújo, J. E., & Castilho, V. M. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00038-x · Cited by 280
Social Stress in Hamsters: Defeat Activates Specific Neurocircuits within the Brain
Kollack‐Walker, S., Watson, S. J., & Akil, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-22-08842.1997 · Cited by 253
Self-citationAnticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats.
Burgdorf, J. S., Knutson, B. D., & Panksepp, J. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.2.320 · Cited by 244
Self-citationForebrain expression of c-fos due to active maternal behaviour in lactating rats
Lonstein, J. S., Simmons, D. A., Swann, J. M., & Stern, J. M. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00283-2 · Cited by 237
PELLIS, S. M., FIELD, E. F., SMITH, L. K., & PELLIS, V. C. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00060-7 · Cited by 234
Effects of neonatal decortication on the social play of juvenile rats
Panksepp, J., Normansell, L., Cox, J. F., & Siviy, S. M. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90285-2 · Cited by 204
Self-citationPlay 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 200
Kinchla, R. A. (1992) · Annual Review of Psychology · doi:10.1146/annurev.ps.43.020192.003431 · Cited by 191
Lonstein, J. S., & Stern, J. M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-09-03364.1997 · Cited by 183
Bandler, R. J., Depaulis, A., & Vergnes, M. (1985) · Behavioural Brain Research · doi:10.1016/0166-4328(85)90058-0 · Cited by 181
Sensory modulation of juvenile play in rats
Siviy, S. M., & Panksepp, J. (1987) · Developmental Psychobiology · doi:10.1002/dev.420200108 · Cited by 181
Self-citationSocial 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
Numan, M., & Numan, M. J. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.1.135 · Cited by 136
Neural substrates of aggression and flight in the cat
Siegel, A., & Pott, C. B. (1988) · Progress in Neurobiology · doi:10.1016/0301-0082(88)90015-9 · Cited by 130
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
Self-citationThe effects of early social isolation on the motivation for social play in juvenile rats
Ikemoto, S., & Panksepp, J. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250404 · Cited by 121
Self-citationKollack‐Walker, Don, Watson, & Akil (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00354.x · Cited by 113
Seeger, T., Sforzo, G. A., Pert, C. B., & Pert, A. (1984) · Brain Research · doi:10.1016/0006-8993(84)90436-0 · Cited by 100
Social play alters regional brain opioid receptor binding in juvenile rats
Vanderschuren, L. J. M. J., Stein, E. A., Wiegant, V. M., & Van Ree, J. M. (1995) · Brain Research · doi:10.1016/0006-8993(95)00256-p · Cited by 88
c-Fos expression in female hamster brain following sexual and aggressive behaviors
Joppa, M. A., Meisel, R. L., & Garber, M. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00179-m · Cited by 68
Pellis, S. M., Castañeda, E., McKenna, M. M., Tran-Nguyen, L. T. L., & Whishaw, I. Q. (1993) · Neuroscience Letters · doi:10.1016/0304-3940(93)90600-p · Cited by 68
Panksepp, J. (1998) · Current Directions in Psychological Science · doi:10.1111/1467-8721.ep10774709 · Cited by 65
Self-citationDorsomedial diencephalic involvement in the juvenile play of rats.
Siviy, S. M., & Panksepp, J. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.6.1103 · Cited by 45
Self-citationMedial hypothalamic lesions and play fighting in juvenile rats.
Beatty, W., & Costello, K. B. (1983) · Physiology and Behavior · doi:10.1016/0031-9384(83)90110-5 · Cited by 17
Pellis, S. M. (1993) · doi:10.1002/1098-2337(1993)19:5
Research works printed but not linked: 1
- Panksepp, 1998, The periconscious substrates of consciousness, J. Consciousness Stud., 5, 566
Cited by
Sorted by citations
Empathy: its ultimate and proximate bases
Preston, S. D., & de Waal, F. B. M. (2002) · Behavioral and Brain Sciences · doi:10.1017/s0140525x02000018 · Cited by 4,126
Consciousness without a cerebral cortex: A challenge for neuroscience and medicine
Merker, B. (2007) · Behavioral and Brain Sciences · doi:10.1017/s0140525x07000891 · Cited by 868
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
Evidence-based Kernels: Fundamental Units of Behavioral Influence
Embry, D. D., & Biglan, A. (2008) · Clinical Child and Family Psychology Review · doi:10.1007/s10567-008-0036-x · Cited by 396
Wöhr, M., & Schwarting, R. K. W. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1607-9 · Cited by 371
Metadata
- Authors
- Gordon, N. S., Kollack-Walker, S., Akil, H., & Panksepp, J.
- Affiliations
- Bowling Green State University (US)
- University of Michigan (US)
- Corresponding author
- Panksepp, Jaak
- Venue
- Brain Research Bulletin
- Publisher
- Elsevier BV
- Published
- 2002-03
- Volume
- 57
- Issue
- 5
- Pages
- 651-659
- ISSN
- 0361-9230 (ISSN-L)
- OpenAlex
- W2078189006
- Cited by
- 103
- References
- 36
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 8 · 2022: 4 · 2021: 2 · 2020: 9 · 2019: 4 · 2018: 6 · 2017: 3 · 2016: 6 · 2015: 5 · 2014: 5 · 2013: 8 · 2012: 2
- FWCI
- 5.97
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research Bulletin (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- rough-and-tumble play, c-fos gene expression, young rats, neuronal activation, brain regions, tectum, inferior colliculus, hypothalamus, striatum, somatosensory cortex, social experience
- MeSH terms
- Aging, Animals, Arousal, Behavior, Animal, Brain, Brain Stem, Male, Motor Activity, Neurons, Play and Playthings, RNA, Messenger, Social Behavior, Up-Regulation, Proto-Oncogene Proteins c-fos, Rats, Long-Evans, 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