Abstract
Despite its apparent adaptive advantages, past research has found that greater familiarity and/or familial relatedness of a social demonstrator does not enhance social learning in the social transmission of food preference paradigm. This finding runs counter to research examining the effects of demonstrator characteristics in fear-mediated social learning paradigms, in which increased familiarity and/or relatedness of a demonstrator promotes higher rates of learning in observer rats. In our first experiment, we were able to corroborate the finding that increased familiarity/relatedness to the demonstrator does not enhance acquisition of a socially transmitted food preference. Furthermore, on examination of the social behavior between observers and their demonstrators during the acquisition of a socially transmitted food preference, no analogous relationship between social contact and expression of the learned preference was observed. In our second experiment, we provide further evidence that familiarity/relatedness may enhance the social acquisition of a fear response to an otherwise neutral auditory cue and demonstrate that this effect is not solely the result of increased social contact between the observer and their demonstrator during acquisition. Despite similar levels of post-cue contact in both observer types, a positive correlation was observed between post-cue social contact and expression of a socially acquired fear behavior when the observer was familiar/related to their demonstrator but not novel/unrelated. These findings both validate previous research on the role of familiarity/relatedness in these two social learning paradigms and provide further behavioral evidence that unique social mechanisms may serve to mediate the social transmission of fear.
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Our data and statistical analyses are readily available at: the University of Texas at Austin data repository, and may be found at the following link: https://dataverse.tdl.org/dataset.xhtml?persistentId=doi:10.18738/T8/0W9TZ9&version=DRAFT.
References
Agee LA, Monfils MH (2018) Effect of demonstrator reliability and recency of last demonstration on acquisition of a socially transmitted food preference. R Soc Open Sci 5:172391. https://doi.org/10.1098/rsos.172391
Bruchey AK, Jones CE, Monfils MH (2010) Fear conditioning by-proxy: social transmission of fear during memory retrieval. Behav Brain Res 214:80–84. https://doi.org/10.1016/j.bbr.2010.04.047
Galef BG (2003) Social learning of food preferences in rodents: rapid appetitive learning. Curr Protoc Neurosci 21(1):8–9. https://doi.org/10.1002/0471142301.ns0805ds21
Galef BG, Laland KN (2005) Social learning in animals: empirical studies and theoretical models. Bioscience 55(6):489–499
Galef BG Jr, Whiskin EE (2000) Demonstration of a socially transmitted flavour aversion in rats? Kuan and Colwill (1997) revisited. Psychon Bull Rev 7:631–635. https://doi.org/10.3758/BF03213000
Galef BG, Whiskin EE (2004) Effects of environmental stability and demonstrator age on social learning of food preferences by young Norway rats. Anim Behav 68:897–902. https://doi.org/10.1016/j.anbehav.2003.10.029
Galef BG, Whiskin EE (2008) Effectiveness of familiar kin and unfamiliar non-kin demonstrator rats in altering food choices of their observers. Anim Behav 76:1381–1388. https://doi.org/10.1016/j.anbehav.2008.07.004
Galef BG Jr, Wigmore SW, Kennett DJ (1983) A failure to find socially mediated taste aversion learning in Norway rats (R. norvegicus). J Comp Psychol 97:358–363
Galef BG Jr, Kennett DJ, Wigmore SW (1984) Transfer of information concerning distant foods in rats: a robust phenomenon. Anim Learn Behav 12:292–296. https://doi.org/10.3758/BF03199970
Galef BG Jr, McQuoid LM, Whiskin EE (1990) Further evidence that Norway rats do not socially transmit learned aversions to toxic baits. Anim Learn Behav 18:199–205. https://doi.org/10.3758/BF03205259
Grover CA, Kixmiller JS, Erickson CA, Becker AH, Davis SF, Nallan GB (1988) The social transmission of information concerning aversively conditioned liquids. Psychol Rec 38:557–566. https://doi.org/10.1007/BF03395047
Guzmán YF, Tronson NC, Guedea A, Huh KH, Gao C, Radulovic J (2009) Social modeling of conditioned fear in mice by non-fearful conspecifics. Behav Brain Res 201(1):173–178. https://doi.org/10.1016/j.bbr.2009.02.024
Jeon D, Kim S, Chetana M, Jo D, Ruley HE, Lin SY, Rabah D, Kinet JP, Shin HS (2010) Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat Neurosci 13:482–488. https://doi.org/10.1038/nn.2504/0/0
Jones CE, Monfils MH (2016a) Dominance status predicts social fear transmission in laboratory rats. Anim Cognit 19:1051–1069. https://doi.org/10.1007/s10071-016-1013-2
Jones CE, Monfils MH (2016b) Post-retrieval extinction in adolescence prevents return of juvenile fear. Learn Mem 23(10):567–575. https://doi.org/10.1101/lm.043281.116
Jones CE, Riha PD, Gore AC, Monfils MH (2014) Social transmission of Pavlovian fear: fear-conditioning by-proxy in related female rats. Anim Cognit 17:827–834. https://doi.org/10.1007/s10071-013-0711-2
Jones CE, Agee LA, Monfils MH (2018) Fear Conditioning by Proxy: social Transmission of Fear Between Interacting Conspecifics. Curr Protoc Neurosci 83(1):e43. https://doi.org/10.1002/cpns.43
Kavaliers M, Colwell DD, Choleris E (2005) Kinship, familiarity and social status modulate social learning about “micropredators” (biting flies) in deer mice. Behav Ecol Sociobiol 58:60–71. https://doi.org/10.1007/s00265-004-0896-0
Kendal RL, Boogert NJ, Rendell L, Laland KN, Webster M, Jones PL (2018) Social Learning Strategies: bridge-Building between Fields. Trends in Cognitive Sci 22(7):651–655. https://doi.org/10.1016/j.tics.2018.04.003
Mathiasen JR, DiCamillo A (2010) Social recognition assay in the rat. Curr Protoc Neurosci. https://doi.org/10.1002/0471142301.ns0805is53
Olsson A, Phelps EA (2007) Social learning of fear. Nat Neurosci 10(9):1095–1102. https://doi.org/10.1038/nn1968
Rendell L, Fogarty L, Hoppitt WJ, Morgan TJ, Webster MM, Laland KN (2011) Cognitive culture: theoretical and empirical insights into social learning strategies. Trends Cognit Sci 15(2):68–76
Saggerson AL, Honey RC (2006) Observational learning of instrumental discriminations in the rat: the role of demonstrator type. Q J Exp Psychol 59(11):1909–1920. https://doi.org/10.1080/17470210600705032
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Research funds obtained through the University of Texas at Austin.
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LAA designed experiment 1, gathered and analyzed data for experiment 1, and drafted the manuscript; CEJ designed experiment 2, gathered and analyzed data for experiment 2, and contributed to writing the manuscript; MHM designed the experiments, interpreted findings, contributed to writing, and approved the final version of this manuscript
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All procedures performed in studies involving animals were in accordance with the ethical standards in accordance with the National Institute of Health’s Guide for the Care and Use of Experimental Animals and were approved by the University of Texas at Austin Animal Care and Use Committee (#2018-00155).
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Agee, L.A., Jones, C.E. & Monfils, MH. Differing effects of familiarity/kinship in the social transmission of fear associations and food preferences in rats. Anim Cogn 22, 1013–1026 (2019). https://doi.org/10.1007/s10071-019-01292-z
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DOI: https://doi.org/10.1007/s10071-019-01292-z