Conspecific interactions predict social transmission of fear in female rats.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
02 Apr 2024
02 Apr 2024
Historique:
received:
17
10
2023
accepted:
27
03
2024
medline:
3
4
2024
pubmed:
3
4
2024
entrez:
2
4
2024
Statut:
epublish
Résumé
Social transmission of fear occurs in a subset of individuals, where an Observer displays a fear response to a previously neutral stimulus after witnessing or interacting with a conspecific Demonstrator during memory retrieval. The conditions under which fear can be acquired socially in rats have received attention in recent years, and suggest that social factors modulate social transmission of information. We previously found that one such factor, social rank, impacts fear conditioning by proxy in male rats. Here, we aimed to investigate whether social roles as determined by nape contacts in females, might also have an influence on social transmission of fear. In-line with previous findings in males, we found that social interactions in the home cage can provide insight into the social relationship between female rats and that these relationships predict the degree of fear acquired by-proxy. These results suggest that play behavior affects the social transfer/transmission of information in female rats.
Identifiants
pubmed: 38565873
doi: 10.1038/s41598-024-58258-6
pii: 10.1038/s41598-024-58258-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7804Informations de copyright
© 2024. The Author(s).
Références
John, E. R., Chesler, P., Bartlett, F. & Victor, I. Observation learning in cats. Science 59, 1489–1491 (1968).
doi: 10.1126/science.159.3822.1489
Hygge, S. & Ohman, A. Modeling processes in the acquisition of fears: Vicarious electrodermal conditioning to fear-relevant stimuli. J. Pers. Soc. Psychol. 36, 271–279 (1978).
pubmed: 650384
doi: 10.1037/0022-3514.36.3.271
Mineka, S. & Cook, M. Mechanisms involved in the observational conditioning of fear. J. Exp. Psychol. Gen. 122, 23–38 (1993).
pubmed: 8440976
doi: 10.1037/0096-3445.122.1.23
Kavaliers, M., Colwell, D. D. & Choleris, E. Kinship, familiarity and social status modulate social learning about “micropredators” (biting flies) in deer mice. Behav. Ecol. Sociobiol. 58, 60–71 (2005).
doi: 10.1007/s00265-004-0896-0
Olsson, A., Nearing, K. I. & Phelps, E. A. Learning fears by observing others: The neural systems of social fear transmission. Soc. Cogn. Affect. Neurosci. 2, 3–11 (2007).
pubmed: 18985115
pmcid: 2555428
doi: 10.1093/scan/nsm005
Gonzalez-Liencres, C., Juckel, G., Tas, C., Friebe, A. & Brüne, M. Emotional contagion in mice: The role of familiarity. Behav. Brain Res. 263, 16–21 (2014).
pubmed: 24480421
doi: 10.1016/j.bbr.2014.01.020
Monfils, M. H. & Agee, L. A. Insights from social transmission of information in rodents. Genes Brain Behav. 18, e12534. https://doi.org/10.1111/gbb.12534 (2019).
doi: 10.1111/gbb.12534
pubmed: 30375171
Agee, L. A., Jones, C. E. & Monfils, M.-H. Differing effects of familiarity/kinship in the social transmission of fear associations and food preferences in rats. Anim. Cogn. 22, 1013–1026 (2019).
pubmed: 31312982
doi: 10.1007/s10071-019-01292-z
Jones, C. E., Riha, P. D., Gore, A. C. & Monfils, M.-H. Social transmission of Pavlovian fear: Fear-conditioning by-proxy in related female rats. Anim. Cogn. 17, 827–834 (2014).
pubmed: 24310150
doi: 10.1007/s10071-013-0711-2
Kiyokawa, Y., Honda, A., Takeuchi, Y. & Mori, Y. A familiar conspecific is more effective than an unfamiliar conspecific for social buffering of conditioned fear responses in male rats. Behav. Brain Res. 267, 189–193 (2014).
pubmed: 24698797
doi: 10.1016/j.bbr.2014.03.043
Pisansky, M. T., Hanson, L. R., Gottesman, I. I. & Gewirtz, J. C. Oxytocin enhances observational fear in mice. Nat. Commun. 8, 2102 (2017).
pubmed: 29235461
pmcid: 5727393
doi: 10.1038/s41467-017-02279-5
Liévin-Bazin, A. et al. Emotional responses to conspecific distress calls are modulated by affiliation in cockatiels (Nymphicus hollandicus). PLoS ONE 13, e0205314. https://doi.org/10.1371/journal.pone.0205314 (2018).
doi: 10.1371/journal.pone.0205314
pubmed: 30300404
pmcid: 6177178
Chen, Q., Panksepp, J. B. & Lahvis, G. P. Empathy is moderated by genetic background in mice. PLoS ONE 4, e4387. https://doi.org/10.1371/journal.pone.0004387 (2009).
doi: 10.1371/journal.pone.0004387
pubmed: 19209221
pmcid: 2633046
Jeon, D. et al. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat. Neurosci. 13, 482–488 (2010).
pubmed: 20190743
pmcid: 2958925
doi: 10.1038/nn.2504
Hirota, Y. et al. Oxytocin receptor antagonist reverses the blunting effect of pair bonding on fear learning in monogamous prairie voles. Horm. Behav. 120, 104685 (2020).
pubmed: 31935400
pmcid: 7117995
doi: 10.1016/j.yhbeh.2020.104685
Jones, C. E. & Monfils, M. H. Dominance status predicts social fear transmission in laboratory rats. Anim. Cogn. 19, 1051–1069 (2016).
pubmed: 27411940
pmcid: 5054054
doi: 10.1007/s10071-016-1013-2
Kendal, R. et al. Chimpanzees copy dominant and knowledgeable individuals: Implications for cultural diversity. Evol. Hum. Behav. 36, 65–72 (2015).
pubmed: 27053916
pmcid: 4820294
doi: 10.1016/j.evolhumbehav.2014.09.002
Pellis, S. M. & Pellis, V. C. Juvenilized play fighting in subordinate male rats. Aggress. Behav. 18, 449–457 (1992).
doi: 10.1002/1098-2337(1992)18:6<449::AID-AB2480180607>3.0.CO;2-T
Adams, N. & Boice, R. A longitudinal study of dominance in an outdoor colony of domestic rats. J. Comp. Psychol. 97, 24–33 (1983).
doi: 10.1037/0735-7036.97.1.24
Ziporyn, T. & McClintock, M. K. Passing as an indicator of social dominance among female wild and domestic Norway rats. Behaviour 118, 26–41 (1991).
doi: 10.1163/156853991X00184
Clarke, F. M. & Faulkes, C. G. Dominance and queen succession in captive colonies of the eusocial naked mole-rat, Heterocephalus glaber. Proc. R. Soc. B 264, 993–1000 (1997).
pubmed: 9263466
pmcid: 1688532
doi: 10.1098/rspb.1997.0137
Parent, C. I., Del Corpo, A., Cameron, N. M. & Meaney, M. J. Maternal care associates with play dominance rank among adult female rats. Dev. Psychobiol. 55, 745–756 (2013).
pubmed: 22786820
doi: 10.1002/dev.21070
Lee, C. T. & Naranjo, J. N. The effects of castration and androgen on the social dominance of BALB/cJ male mice. Physiol. Psychol. 2, 93–98 (1974).
doi: 10.3758/BF03333000
Benton, D., Dalrymplealford, J. C. & Brain, P. F. Comparisons of measures of dominance in the laboratory mouse. Anim. Behav. 28, 1274–1279 (1980).
doi: 10.1016/S0003-3472(80)80115-1
So, N., Franks, B., Lim, S. & Curley, J. P. A social network approach reveals associations between mouse social dominance and brain gene expression. PLoS One 10, e0134509. https://doi.org/10.1371/journal.pone.0134509 (2015).
doi: 10.1371/journal.pone.0134509
pubmed: 26226265
pmcid: 4520683
Williamson, C. M., Lee, W. & Curley, J. P. Temporal dynamics of social hierarchy formation and maintenance in male mice. Anim. Behav. 115, 259–272 (2016).
doi: 10.1016/j.anbehav.2016.03.004
Williamson, C. M. et al. Social hierarchy position in female mice is associated with plasma corticosterone levels and hypothalamic gene expression. Sci. Rep. 9, 7324 (2019).
pubmed: 31086272
pmcid: 6513839
doi: 10.1038/s41598-019-43747-w
Pellis, S. M. & Pellis, V. C. On knowing it’s only play: The role of play signals in play fighting. Aggress. Viol. Behav. 1, 249–268 (1996).
doi: 10.1016/1359-1789(95)00016-X
Pellis, S. M., Field, E. F., Smith, L. K. & Pellis, V. C. Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neurosci. Biobehav. Rev. 21, 105–120 (1997).
pubmed: 8994213
doi: 10.1016/0149-7634(95)00060-7
Marquardt, A. E., VanRyzin, J. W., Fuquen, R. W. & McCarthy, M. M. Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females. Front. Behav. Neurosci. 16, 1076765 (2023).
pubmed: 36755666
pmcid: 9899815
doi: 10.3389/fnbeh.2022.1076765
Smith, L. K., Field, E. F., Forgie, M. L. & Pellis, S. M. Dominance and age-related changes in the play fighting of intact and post-weaning castrated male rats (Rattus norvegicus). Aggress. Behav. 22, 215–226 (1996).
doi: 10.1002/(SICI)1098-2337(1996)22:3<215::AID-AB6>3.0.CO;2-L
Kamitakahara, H., Monfils, M. H., Forgie, M. L., Kolb, B. & Pellis, S. M. The modulation of play fighting in rats: Role of the motor cortex. Behav. Neuro. 121, 164–176 (2007).
doi: 10.1037/0735-7044.121.1.164
Bell, H. C., McCaffrey, D. R., Forgie, M. L., Kolb, B. & Pellis, S. M. The role of the medial prefrontal cortex in the play fighting of rats. Behav. Neurosci. 123, 1158–1168 (2009).
pubmed: 20001100
doi: 10.1037/a0017617
Himmler, B. T., Pellis, V. C. & Pellis, S. M. Peering into the dynamics of social interactions: Measuring play fighting in rats. J. Vis. Exp. 71, e4288 (2013).
Schweinfurth, M. K. et al. Do female Norway rats form social bonds?. Behav. Ecol. Sociobiol. 71, 98 (2017).
doi: 10.1007/s00265-017-2324-2
Schweinfurth, M. K., Stieger, B. & Taborsky, M. Experimental evidence for reciprocity in allogrooming among wild-type Norway rats. Sci. Rep. 7, 4010 (2017).
pubmed: 28638051
pmcid: 5479849
doi: 10.1038/s41598-017-03841-3
Fang, J. & Clemens, L. G. Contextual determinants of female-female mounting in laboratory rats. Anim. Behav. 57, 545–555 (1999).
pubmed: 10196044
doi: 10.1006/anbe.1998.1025
Blanchard, D. C., Fukunaga-Stinson, C., Takahashi, L. K., Flannelly, K. J. & Blanchard, R. J. Dominance and aggression in social groups of male and female rats. Behav. Process. 9, 31–48 (1984).
doi: 10.1016/0376-6357(84)90006-8
Redecker, T. M., Kisko, T. M., Schwarting, R. K. W. & Wöhr, M. Effects of Cacna1c haploinsufficiency on social interaction behavior and 50-kHz ultrasonic vocalizations in adult female rats. Behav. Brain Res. 367, 35–52 (2019).
pubmed: 30902660
doi: 10.1016/j.bbr.2019.03.032
Calhoun, J. B. The Ecology and Sociology of the Norway Rat (U.S. Dept. of Health, Education and Welfare, Public Health Service, 1963).
doi: 10.5962/bhl.title.112283
Bruchey, A. K., Jones, C. E. & Monfils, M.-H. Fear conditioning by-proxy: Social transmission of fear during memory retrieval. Behav. Brain Res. 214, 80–84 (2010).
pubmed: 20441779
pmcid: 2975564
doi: 10.1016/j.bbr.2010.04.047
Goldman, J. M., Murr, A. S. & Cooper, R. L. The rodent estrous cycle: Characterization of vaginal cytology and its utility in toxicological studies. Dev. Reprod. Toxicol. 80, 84–97 (2007).
Westwood, F. R. The female rat reproductive cycle: A practical histological guide to staging. Toxicol. Pathol. 36, 375–384 (2008).
pubmed: 18441260
doi: 10.1177/0192623308315665
Venables, W. N. & Ripley, B. D. Modern applied statistics with S 4th edn. (Springer, 2002).
doi: 10.1007/978-0-387-21706-2
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2020).
Fox, J. & Hong, J. Effect displays in R for multinomial and proportional-odds logit models: Extensions to the effects package. J. Stat. Softw. 32, 1–24. https://doi.org/10.18637/jss.v032.i01 (2009).
doi: 10.18637/jss.v032.i01
Fox, J. & Weisberg, S. Visualizing fit and lack of fit in complex regression models with predictor effect plots and partial residuals. J. Stat. Softw. 87, 1–27 (2018).
doi: 10.18637/jss.v087.i09
Fox, J. & Weisberg, S. An R Companion to Applied Regression 3rd edn. (SAGE Publications, 2019).
Kleiber, C. & Zeileis, A. Applied Econometrics with R (Springer-Verlag, 2008).
doi: 10.1007/978-0-387-77318-6
Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
doi: 10.18637/jss.v067.i01
Pellis, S. M. & Pellis, V. C. Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Dev. Psychobiol. 23, 215–231 (1990).
pubmed: 2379760
doi: 10.1002/dev.420230303
Meaney, M. J. & Stewart, J. A descriptive study of social development in the rat (Rattus norvegicus). Anim. Behav. 29, 34–45 (1981).
doi: 10.1016/S0003-3472(81)80149-2
Meaney, M. J. & Stewart, J. Neonatal-androgens influence the social play of prepubescent rats. Horm. Behav. 15, 197–213 (1981).
pubmed: 7250910
doi: 10.1016/0018-506X(81)90028-3
Byers, S. L., Wiles, M. V., Dunn, S. L. & Taft, R. A. Mouse estrous cycle identification tool and images. PLoS One 7, e35538 (2012).
pubmed: 22514749
pmcid: 3325956
doi: 10.1371/journal.pone.0035538
Siviy, S. M. & Panksepp, J. Sensory modulation of juvenile play in rats. Dev. Psychobiol. 20, 39–55 (1987).
pubmed: 3556783
doi: 10.1002/dev.420200108
Whishaw, I. Q., Pellis, S. M. & Pellis, V. C. A behavioral study of the contributions of cells and fibers of passage in the red nucleus of the rat to postural righting, skilled movements, and learning. Behav. Brain Res. 52, 29–44 (1992).
pubmed: 1472285
doi: 10.1016/S0166-4328(05)80322-5
Smith, P. K. Does play matter? Functional and evolutionary aspects of animal and human play. Behav. Brain Sci. 5, 139–184 (1982).
doi: 10.1017/S0140525X0001092X
Pellis, S. M. & Pellis, V. C. Some subordinates are more equal than others: Play fighting amongst adult subordinate male rats. Aggress. Behav. 19, 385–393 (1993).
doi: 10.1002/1098-2337(1993)19:5<385::AID-AB2480190508>3.0.CO;2-#
Blair, R. S. et al. Estrous cycle contributes to state-dependent contextual fear in female rats. Psychoneuroendocrinology 141, 105776 (2022).
pubmed: 35489312
doi: 10.1016/j.psyneuen.2022.105776