Deprivation of direct adult contact during development affects social representation in a songbird.
adult influences
operant conditioning
social cognition
social deprivation
social motivation
social representation
Journal
Developmental psychobiology
ISSN: 1098-2302
Titre abrégé: Dev Psychobiol
Pays: United States
ID NLM: 0164074
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
revised:
23
09
2021
received:
19
04
2021
accepted:
24
09
2021
entrez:
23
11
2021
pubmed:
24
11
2021
medline:
26
3
2022
Statut:
ppublish
Résumé
Social cognition involves a wide array of skills that are built largely through interactions with conspecifics and therefore depend upon early social experience. Motivation for social stimuli is a key feature of social behavior and an operant conditioning task showed that isolated wild-caught adult starlings (Sturnus vulgaris) are highly motivated to access pictures of other starlings. Here, we show that hand-raised adult starlings maintained in groups of peers throughout development but without any contact with adult models were not or only poorly motivated to access pictures of conspecifics. Moreover, they did not prefer pictures of starlings to pictures of landscapes, unlike birds wild-caught as adults. These results raise questions about the role of social experience during development, particularly with adult models, in the development of social motivation and of social representation in general.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e22207Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Adret, P. (1993). Operant conditioning, song learning and imprinting to taped song in the zebra finch. Animal Behaviour, 46, 149-159.
Appeltants, D., Gentner, T., Hulse, S. H., Balthazart, J., & Ball, G. F. (2005). The effect of auditory distractors on song discrimination in male canaries (Serinus canaria). Behavioural Processes, 69, 331-341.
Arnold, C., & Taborsky, B. (2010). Social experience in early ontogeny has lasting effects on social skills in cooperatively breeding cichlids. Animal Behaviour, 79, 621-630. https://doi.org/10.1016/j.anbehav.2009.12.008
Bertin, A., Hausberger, M., Henry, L., & Richard-Yris, M. A. (2007). Adult and peer influences on starling song development. Developmental Psychobiology, 49, 362-374.
Bertin, A., Hausberger, M., Henry, L., & Richard-Yris, M. A. (2009). Adult: Young ratio influences song acquisition in female European starlings (Sturnus vulgaris). Journal of Comparative Psychology, 123, 195-203. https://doi.org/10.1037/a0014050
Boogert, N. J., Lachlan, R. F., Spencer, K. A., Templeton, C. N., & Farine, D. R. (2018). Stress hormones, social associations and song learning in zebra finches. Philosophical Transactions of the Royal Society. B, Biological Sciences, 373, 20170290. https://doi.org/10.1098/rstb.2017.0290
Borland, J. M., Frantz, K. J., Aiani, L. M., Grantham, K. N., Song, Z., & Albers, H. E. (2017). A novel operant task to assess social reward and motivation in rodents. Journal of Neuroscience Methods, 287, 80-88.
Boucherie, P. H., Loretto, M.-C., Massen, J. J. M., & Bugnyar, T. (2019). What constitutes « social complexity » and « social intelligence » in birds? Lessons from ravens. Behavioral Ecology and Sociobiology, 73(1), 12. https://doi.org/10.1007/s00265-018-2607-2
Bouet, V., Lecrux, B., Tran, G., & Freret, T. (2011). Effect of pre- versus post-weaning environmental disturbances on social behaviour in mice. Neuroscience Letters, 488, 221-224. https://doi.org/10.1016/j.neulet.2010.11.033
Bourjade, M., de Boyer des Roches, A., & Hausberger, M. (2009). Adult-young ratio, a major factor regulating social behaviour of young: A horse study. PLoS One, 4, e4888.
Bourjade, M., Moulinot, M., Henry, S., Richard-Yris, M. A., & Hausberger, M. (2008). Could adults be used to improve social skills of young horses, Equus caballus? Developmental Psychobiology, 50, 408-417.
Caskey, M., Stephens, B., Tucker, R., & Vohr, B. (2011). Importance of parent talk on the development of preterm infant vocalizations. Pediatrics, 128, 910-916.
Chen, Y., Matheson, L. E., & Sakata, J. T. (2016). Mechanisms underlying the social enhancement of vocal learning in songbirds. Proceedings of the National Academy of Sciences of the United States of America, 113, 6641-6646.
Christensen, J. W., Ladewig, J., Søndergaard, E., & Malmkvist, J. (2002). Effects of individual versus group stabling on social behaviour in domestic stallions. Applied Animal Behaviour Science, 75(3), 233-248. https://doi.org/10.1016/S0168-1591(01)00196-4
Collins, S. A. (1999). Is female preference for male repertoires due to sensory bias. Proceedings of the Royal Society B, 266, 2309-2314.
Contreras-Huerta, L. S., Lockwood, P. L., Bird, G., Apps, M. A. J., & Crockett, M. J. (2020). Prosocial behavior is associated with transdiagnostic markers of affective sensitivity in multiple domains. Emotion (Washington, D.C.), https://doi.org/10.1037/emo0000813
Cousillas, H., Richard, J.-P., Mathelier, M., Henry, L., George, I., & Hausberger, M. (2004). Experience-dependent neuronal specialization and functional organization in the central auditory area of a songbird. European Journal of Neuroscience, 19(12), 3343-3352. https://doi.org/10.1111/j.0953-816X.2004.03376.x
Cousillas, H., George, I., Henry, L., Richard, J. P., & Hausberger, M. (2008). Linking social and vocal brains: Could social segregation prevent a proper development of a central auditory area in a female songbird? PLoS One, 3, e2194.
Cousillas, H., George, I., Mathelier, M., Richard, J. P., Henry, L., & Hausberger, M. (2006). Social experience influences the development of a central auditory area. Die Naturwissenschaften, 93, 588-596.
Cronin, K. A. (2012). Prosocial behaviour in animals : The influence of social relationships, communication and rewards. Animal Behaviour, 84(5), 1085-1093. https://doi.org/10.1016/j.anbehav.2012.08.009
Duque, J. F., Leichner, W., Ahmann, H., & Stevens, J. R. (2018). Mesotocin influences pinyon jay prosociality. Biology Letters, 14(4), 20180105. https://doi.org/10.1098/rsbl.2018.0105
Duque, J. F., Rasmussen, T., Rodriguez, A. & Stevens, J. R. (2019). The role of mesotocin on social bonding in pinyon jays. Ethology 126, 165-175. https://www.biorxiv.org/content/10.1101/599555v2
Feare, C. (1984). The Starling. Oxford: Oxford University Press.
Frith, C. D. (2008). Social cognition. Philosophical Transactions of the Royal Society B, 363, 2033-2039. https://doi.org/10.1098/rstb.2008.0005
George, I., Alcaix, S., Henry, L., Richard, J.-P., Cousillas, H., & Hausberger, M. (2010). Neural correlates of experience-induced deficits in learned vocal communication. PLoS One, 5(12), e14347. https://doi.org/10.1371/journal.pone.0014347
George, I., Richard, J.-P., Cousillas, H., & Hausberger, M. (2011). No need to talk, I know you: Familiarity influences early multisensory integration in a Songbird's brain. Frontiers in Behavioral Neuroscience, 4, 193. https://doi.org/10.3389/fnbeh.2010.00193
George, I., Cousillas, H., Richard, J. P., & Hausberger, M. (2012). Experience with adults shapes multisensory representation of social familiarity in the brain of a songbird. PLoS One, 7, e38764. doi: https://doi.org/10.1371/journal.pone.0038764
Goldstein, M. H., King, A. P., & West, M. J. (2003). Social interaction shapes babbling: Testing parallels between birdsong and speech. Proceedings of the National Academy of Sciences of the United States of America, 100, 8030-8035.
Halperin, J. R. P., & Dunham, D. W. (1993). Increased aggressiveness after brief social isolation of adult fish: A connectionist model which organizes this literature. Behavioral Processes, 28, 123-l44.
Hausberger, M., Richard-Yris, M.-A., Henry, L., Lepage, L., & Schmidt, I. (1995). Song sharing reflects the social-organization in a captive group of European Starlings (sturnus-Vulgaris). Journal of Comparative Psychology, 109(3), 222-241. https://doi.org/10.1037//0735-7036.109.3.222
Henry, L., Le Cars, K., Mathelier, M., Bruderer, C., & Hausberger, M. (2008). The use of a mirror as a `social substitute’ in laboratory birds. Comptes Rendus Biologies, 331, 526-531.
Henry, L., Bourguet, C., Coulon, M., Aubry, C., & Hausberger, M. (2013). Sharing mates and nest boxes is associated with female “friendship” in European starlings, Sturnus vulgaris. Journal of Comparative Psychology, 127(1), 1-13. https://doi.org/10.1037/a0029975
Henry, S., Zanella, A. J., Sankey, C., Richard-Yris, M. A., Marko, A., & Hausberger, M. (2012). Adults may be used to alleviate weaning stress in domestic foals (Equus caballus). Physiology & Behavior, 106, 428-438.
Hesse, S., & Thünken, T. (2014). Growth and social behavior in a cichlid fish are affected by social rearing environment and kinship. Die Naturwissenschaften, 101, 273-283. https://doi.org/10.1007/s00114-014-1154-6
Hewlett, S. E., Wareham, D. M., & Barron, A. B. (2018). Honey bee (Apis mellifera) sociability and nestmate affiliation are dependent on the social environment experienced post-eclosion. Journal of Experimental Biology, 221, jeb173054. https://doi.org/10.1242/jeb.173054
Kaplan, G. (2020). Long-term attachments and complex cognition in birds and humans are linked to pre-reproductive prosociality and cooperation. Constructing a hypothesis. Annals of Cognitive Science, 4(1),. https://scholars.direct/Articles/cognitive-science/acs-4-015.php?jid=cognitive-science
Kuhl, P. K., Tsao, F. M., & Liu, H. M. (2003). Foreign-language experience in infancy: Effects of short-term exposure and social interaction on phonetic learning. Proceedings of National Academy of Science of the United States of America, 100, 9096-9101.
Lehongre, K., Lenouvel, P., Draganoiu, T., & Del Negro, C. (2006). Long-term effect of isolation rearing conditions on songs of an ‘open-ended’ song learner species, the canary. Animal Behaviour, 72, 1319-1327. https://doi.org/10.1016/j.anbehav.2006.03.025
Lemasson, A., Gautier, J. P., & Hausberger, M. (2005). A brief note on the effects of the removal of individuals on social behaviour in a captive group of campbell's monkeys (Cercopithecus campbelli campbelli): A case study. Applied Animal Behaviour Science, 91, 289-296.
Marshall-Pescini, S., Dale, R., Quervel-Chaumette, M., & Range, F. (2016). Critical issues in experimental studies of prosociality in non-human species. Animal Cognition, 19(4), 679-705. https://doi.org/10.1007/s10071-016-0973-6
McComb, K., Moss, C., Durant, S. M., Baker, L., & Sayialel, S. (2001). Matriarchs as repositories of social knowledge in African elephants. Science, 292, 491-494.
Nettle, D., Andrews, C. P., Monaghan, P., Brilot, B. O., Bedford, T., Gillespie, R., & Bateson, M. (2015), Developmental and familial predictors of adult cognitive traits in the European starling. Animal Behaviour, 107, 239-248. https://doi.org/10.1016/j.anbehav.2015.07.002
Okanoya, K., & Tsumaki, S., & Honda, E. (2000). Perception of temporal properties in self-generated songs by Bengalese finches (Lonchura striata var. domestica). Journal of Comparative Psychology, 114, 239-245.
Olmstead, M. C., & Kuhlmeier, V. A. (2015). Comparative Cognition. Cambridge: Cambridge University Press.
Perré, Y., Wauters, A.-M., & Richard-Yris, M.-A. (2002). Influence of mothering on emotional and social reactivity of domestic pullets. Applied Animal Behaviour Science, 75(2), 133-146. https://doi.org/10.1016/S0168-1591(01)00189-7
Perret, A., Henry, L., Coulon, M., Caudal, J. P., Richard, J. P., Cousillas, H., Hausberger, M., & George, I. (2015). Social visual contact, a primary “drive” for social animals. Animal Cognition, 18, 657-666. (https://doi.org/10.1007/s10071-015-0834-8)
Poirier, C., Henry, L., Mathelier, M., Lumineau, S., Cousillas, H., & Hausberger, M. (2004). Direct social contacts override auditory information in the song-learning process in starlings (Sturnus vulgaris). Journal of Comparative Psychology, 118, 179-193.
Ros-Simo, C., & Valverde, O. (2012). Early-life social experiences in mice affect emotional behaviour and hypothalamic-pituitary-adrenal axis function. Pharmacology Biochemistry and Behavior, 102, 434-441.
Santos, M. J., Merlo, S. A., Kaczer, L., & Pedreira, M. E. (2021). Social context shapes cognitive abilities: Associative memories are modulated by fight outcome and social isolation in the crab Neohelice granulata. Animal Cognition, 24(5), 1007-1026. https://doi.org/10.1007/s10071-021-01492-6
Slotow, R., van Dyk, G., Poole, J., Page, B., & Klocke, A. (2000). Older bull elephants control young males. Nature, 408, 425-426.
Snowdon, C. T., & Hausberger, M. (1997). Social Influences on Vocal Development. Cambridge, Cambridge University Press.
Taborsky, B., & Oliveira, R. F. (2012). Social competence: An evolutionary approach. Trends in Ecology & Evolution, 27, 679-688.
Teitelbaum, C. S., Converse, S. J., & Mueller, T. (2017). Birds choose long-term partners years before breeding. Animal Behaviour, 134, 147-154.
Templer, V. L., Wise, T. B., Dayaw, K. I. T., & Dayaw, J. N. T. (2018). Nonsocially housed rats (Ratus norvegicus) seek social interactions and social novelty more than socially housed counterparts. Journal of Comparative Psychology, 132, 240-252.
Tóth, M., Halász, J., Mikics, E., Barsy, B., & Haller, J. (2008). Early social deprivation induces disturbed social communication and violent aggression in adulthood. Behavioral Neuroscience, 122, 849-854. https://doi.org/10.1037/0735-7044.122.4.849
Ward, A., & Webster, M. (2016), Sociality: The Behaviour of Group-Living Animals. Cham: Springer.
Weiler, N. (2015). Lonely starlings stare at strangers. https://doi.org/10.1126/science.aaa6413