Multisensory interaction mediates the social transmission of avoidance in rats: Dissociation from social transmission of fear
Abstract
Social interaction enables animals to transmit various types of sensory information that can modulate learned avoidance behavior and fear responses, which are important to survival. We previously reported that, under a passive avoidance paradigm, avoidance behavior is facilitated when a rat observes another rat (demonstrator) receiving a shock when performing a specific behavior. However, the sensory mechanisms underlying this 'social facilitation of avoidance' are not well understood. The present study examined the role of sensory pathways for social transmission of avoidance, focusing on the olfactory and visual systems. The olfactory ability of observer rats was blocked by an intranasal application of ZnSO4, and their visual ability was blocked by an opaque partition placed between observer and demonstrator rats. We found that blocking either olfactory or visual input drastically diminished the social transmission of avoidance. Interestingly the social transmission of fear responses remained intact even when olfactory or visual information was blocked. These results indicate that the social transmission of avoidance is mediated not by any single sensory modality but by multisensory interaction in rats, suggesting a distinct sensory mechanism from that underlying the social transmission of fear.
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Masuda et al. showed that social learning of avoidance depends on both visual and olfactory cues.
“Further, Masuda et al showed that social learning of avoidance depends on both visual and olfactory cues.174”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [174]
Responses of observers can be elicited by rapid, random body movements, as well as the lack of movement.
“Responses of the observers can be also elicited by rapid, random body movements, 152,174 as well as the lack of movement.175”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [174]
Cites
SOCIAL LEARNING IN ANIMALS: CATEGORIES AND MECHANISMS
Heyes, C. M. (1994) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1994.tb01506.x · Cited by 1,023 · see citing works
Molholm, S., Ritter, W., Murray, M. M., Javitt, D., Schroeder, C., & Foxe, J. J. (2002) · Brain research. Cognitive brain research · doi:10.1016/s0926-6410(02)00066-6 · Cited by 980 · see citing works
Social Modulation of Pain as Evidence for Empathy in Mice
Langford, D. J., Crager, S. E., Shehzad, Z., Smith, S. B., Sotocinal, S. G., Levenstadt, J. S., Chanda, M. L., Levitin, D. J., & Mogil, J. S. (2006) · Science · doi:10.1126/science.1128322 · Cited by 865 · see citing works
Social Learning in Animals: Empirical Studies and Theoretical Models
Galef, B. G., & Laland, K. N. (2005) · BioScience · doi:10.1641/0006-3568(2005)055[0489:sliaes]2.0.co;2 · Cited by 670 · see citing works
Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC
Jeon, D., Kim, S., Chetana, M., Jo, D., Ruley, H. E., Lin, S.-Y., Rabah, D., Kinet, J.-P., & Shin, H.-S. (2010) · Nature Neuroscience · doi:10.1038/nn.2504 · Cited by 651 · see citing works
Blanchard, R. J., Blanchard, D. C., Agullana, R., & Weiss, S. M. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90423-l · Cited by 461 · see citing works
Foxe, J. J., Mórocz, I. Á., Murray, M. M., Higgins, B. A., Javitt, D. C., & Schroeder, C. E. (2000) · Cognitive Brain Research · doi:10.1016/s0926-6410(00)00024-0 · Cited by 391 · see citing works
Spehr, M., Kelliher, K. R., Li, X., Boehm, T. L. J., Leinders‐Zufall, T., & Zufall, F. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4939-05.2006 · Cited by 301 · see citing works
Mice: Individual Recognition by Olfactory Cues
Bowers, J. M., & ALEXANDER, B. K. (1967) · Science · doi:10.1126/science.158.3805.1208 · Cited by 257 · see citing works
Social Transmission of Fear in Rats: The Role of 22-kHz Ultrasonic Distress Vocalization
Kim, E. J., Kim, E. S., Covey, E., & Kim, J. J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015077 · Cited by 216 · see citing works
Bolognini, N., Frassinetti, F., Serino, A., & Làdavas, E. (2004) · Experimental Brain Research · doi:10.1007/s00221-004-2005-z · Cited by 209 · see citing works
Odor-guided behavior in mammals
Doty, R. (1986) · Experientia · doi:10.1007/bf01942506 · Cited by 201 · see citing works
The social transmission of information and behaviour
Nicol, C. J. (1995) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(95)00607-t · Cited by 200 · see citing works
Borta, A., Wöhr, M., & Schwarting, R. K. W. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.08.009 · Cited by 173 · see citing works
Observational Learning and Social Facilitation in the Rat
Zentall, T. R., & Levine, J. M. (1972) · Science · doi:10.1126/science.178.4066.1220 · Cited by 143 · see citing works
Animal cognition and the rat olfactory system
Slotnick, B. M. (2001) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01625-9 · Cited by 138 · see citing works
No direction-specific bimodal facilitation for audiovisual motion detection
Alais, D., & Burr, D. C. (2004) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2003.11.011 · Cited by 119 · see citing works
Leggio, M. G., Molinari, M., Neri, P. E., Graziano, A., Mandolesi, L., & Petrosini, L. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.040554297 · Cited by 110 · see citing works
Main olfactory system mediates social buffering of conditioned fear responses in male rats
Kiyokawa, Y., Takeuchi, Y., Nishihara, M., & Mori, Y. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06618.x · Cited by 102 · see citing works
Role of the main olfactory system in recognition between individual spiny mice
Matochik, J. A. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90073-x · Cited by 59 · see citing works
The sources of odors from stressed rats
Mackay‐Sim, A., & Laing, D. G. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90340-1 · Cited by 51 · see citing works
Alarm Pheromone that Aggravates Stress-induced Hyperthermia is Soluble in Water
Kiyokawa, Y., Kikusui, T., Takeuchi, Y., & Mori, Y. (2005) · Chemical Senses · doi:10.1093/chemse/bji044 · Cited by 38 · see citing works
Social modulation in extinction of aversive memories
Nowak, A., Werka, T., & Knapska, E. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.031 · Cited by 36 · see citing works
Social Transmission of Avoidance Behavior under Situational Change in Learned and Unlearned Rats
Masuda, A., & Aou, S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006794 · Cited by 33 · see citing works
Self-citationLesions of the medial prefrontal cortex enhance social modulation of avoidance
Masuda, A., & Aou, S. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.10.031 · Cited by 5 · see citing works
Self-citation(2014) · Institutional Repository University of Antioquia (University of Antioquia) · doi:10.1371/journal.pone
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Social Fear Learning: from Animal Models to Human Function
Debiec, J., & Olsson, A. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.04.010 · Cited by 186 · see citing works
Ecological validity of social interaction tests in rats and mice
Kondrakiewicz, K., Kostecki, M., Szadzińska, W., & Knapska, E. (2019) · Genes, Brain and Behavior · doi:10.1111/gbb.12525 · Cited by 136 · see citing works
Sex differences in social modulation of learning in rats
Mikosz, M., Nowak, A., Werka, T., & Knapska, E. (2015) · Scientific Reports · doi:10.1038/srep18114 · Cited by 59 · see citing works
Towards a unified theory of emotional contagion in rodents—A meta-analysis
Hernandez-Lallement, J., Gómez-Sotres, P., & Carrillo, M. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.010 · Cited by 53 · see citing works
Social rejection following neonatal inflammation is mediated by olfactory scent cues
MacRae, M., Kenkel, W. M., & Kentner, A. C. (2015) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2015.02.026 · Cited by 19 · see citing works
- Authors
- Masuda, A., Narikiyo, K., Someya, N., & Aou, S.
- Affiliations
- Kyushu Institute of Technology (JP)
- Japan Society for the Promotion of Science (JP)
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2013-09
- Volume
- 252
- Pages
- 334-338
- ISSN
- 0166-4328 (ISSN-L)
- OpenAlex
- W2035235091
- Cited by
- 6
- References
- 26
- Citations by year
- 2020: 1 · 2018: 2 · 2017: 1 · 2015: 2
- FWCI
- 0.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- multisensory interaction, olfactory input, visual input, zinc sulfate, passive avoidance, observational learning, rats
- MeSH terms
- Afferent Pathways, Animals, Astringents, Avoidance Learning, Conditioning, Classical, Electroshock, Extinction, Psychological, Fear, Male, Odorants, Smell, Social Behavior, Rats, Wistar, Zinc Sulfate, Freezing Reaction, Cataleptic, Rats
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