Cited by 95Autism Spectrum Disorder ResearchNeuroendocrine regulation and behaviorGenetics and Neurodevelopmental Disorders

Olfactory cues are sufficient to elicit social approach behaviors but not social transmission of food preference in C57BL/6J mice

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Ryan, Bryce C., Young, Nancy B., Moy, Sheryl S., Crawley, Jacqueline N.·2008·Behavioural Brain Research

Abstract

Mouse models for the study of autistic-like behaviors are increasingly needed to test hypotheses about the causes of autism, and to evaluate potential treatments. Both the automated three-chambered social approach test and social transmission of food preference have been proposed as mouse behavioral assays with face validity to diagnostic symptoms of autism, including aberrant reciprocal social interactions and impaired communication. Both assays measure aspects of normal social behavior in the mouse. However, little is known regarding the salient cues present in each assay that elicit normal social approach and communication. To deconstruct the critical components, we focused on delivering discrete social and non-social olfactory and visual cues within the context of each assay. Results indicate that social olfactory cues were sufficient to elicit normal sociability in the three-chambered social approach test. On social transmission of food preference, isolated social olfactory cues were sufficient to induce social investigation, but not sufficient to induce food preference. These findings indicate that olfactory cues are important in mouse social interaction, but that additional sensory cues are necessary in certain situations. The present evidence that both the three-chambered social approach assay and the social transmission of food preference assay require socially relevant cues to elicit normal behavior supports the use of these two assays to investigate autism-related behavioral phenotypes in mice.

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Crossref · 10.1016/j.bbr.2008.06.002

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  • Ryan and co-workers showed that male C57BL/6J mice in the three-chambered apparatus test displayed equal amount of interest in the stimulus animal independent of its sex.

    “Ryan and co-workers showed that male C57BL/6J mice in the three-chambered apparatus test displayed equal amount of interest in the stimulus animal independent of its sex [27].”

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Research works printed but not linked: 56

  1. Ahl AS. The role of vibrissae in behavior: a status review. Vet Res Commun 1986;10:245-268. [PubMed: 3526705]
  2. Alberts JR. Producing and interpreting experimental olfactory deficits. Physiol Behav 1974;12:657- 670. [PubMed: 4207423]
  3. Arakawa H, Arakawa K, Blanchard DC, Blanchard RJ. Scent marking behavior in male C57BL/6J mice: sexual and developmental determination. Behav Brain Res 2007;182:73-79. [PubMed: 17561279]
  4. Beauchamp GK, Yamazaki K. Chemical signaling in mice. Biochem Soc Trans 2003;31:147-151. [PubMed: 12546673]
  5. Beauchamp GK, Yamazaki K. Individual differences and the chemical senses. Chem Senses 2005;30:i6-i9. [PubMed: 15738195]
  6. Blanchard RJ, Dulloog L, Markham C, Nishimura O, Compton JN, Jun A, Han C, Blanchard DC. Sexual and aggressive interactions in a visible burrow system with provisioned burrows. Physiol Behav 2001;72:245-254. [PubMed: 11240003]
  7. Bolivar VJ, Walters SR, Phoenix JL. Assessing autism-like behaviors in mice: variations in social interactions among inbred strains. Behav Brain Res 2007;176:21-26. [PubMed: 17097158]
  8. Brennan PA, Kendrick KM. Mammalian social odours: attraction and individual recognition. Philos Trans R Soc Lond B Biol Sci 2006;361:2061-2078. [PubMed: 17118924]
  9. Brennan PA, Zufall F. Pheromonal communication in vertebrates. Nature 2006;444:308-315. [PubMed: 17108955]
  10. Broad KD, Keverne EB. More to pheromones than meets the nose. Nature Neurosci 2008;11:128- 129. [PubMed: 18227795]
  11. Brodkin ES. BALB/c mice: low sociability and other phenotypes that may be relevant to autism. Behav Brain Res 2007;176:53-65. [PubMed: 16890300]
  12. Bunsey M, Eichenbaum H. Selective damage to the hippocampal region blocks long-term retention of a natural and non-spatial stimulus-stimulus association. Hippocampus 1995;5:546-556. [PubMed: 8646281]
  13. Carter CS. Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders? Behav Brain Res 2007;176:170-186. [PubMed: 17000015]
  14. Crawley JN. Designing mouse behavioral tasks relevant to autistic-like behaviors. Ment Retard Dev Disabil Res Rev 2004;10:248-258. [PubMed: 15666335]
  15. Ehret G. Infant rodent ultrasounds -a gate to the understanding of sound communication. Behav Genet 2005;35:19-29. [PubMed: 15674530]
  16. Ferguson JN, Young LJ, Insel TR. The neuroendocrine basis of social recognition. Front Neuroendocrinol 2002;23:200-224. [PubMed: 11950245]
  17. Galef BG Jr, Mason JR, Preti G, Bean NJ. Carbon disulfide: a semiochemical mediating socially- induced diet choice in rats. Physiol Behav 1988;42:119-124. [PubMed: 3368530]
  18. Galef BG Jr, Kennett DJ. Different mechanisms for social transmission of food preference in rat pups of different ages. Dev Psychobiol 1987;20:209-215. [PubMed: 3582781]
  19. Galef BG Jr, Whiskin EE. Socially transmitted food preference can be used to study long-term memory in rats. Learn Behav 2003;31:160-164. [PubMed: 12882374]
  20. Galef BG Jr, Wigmore SW, Kennett DJ. A failure to find socially mediated taste aversion learning in Norway rats (R. norvegicus). J Comp Psychol 1983;97:358-363. [PubMed: 6317281]
  21. Hahn ME, Lavooy MJ. A review of the methods of studies on infant ultrasound production and maternal retrieval in small rodents. Behav Genet 2005;35:31-52. [PubMed: 15674531]
  22. Hammock EA, Young LJ. Oxytocin, vasopressin and pair bonding: implications for autism. Philos Trans R Soc Lond B Biol Sci 2006;361:2187-2198. [PubMed: 17118932]
  23. Holy TE, Guo Z. Ultrasonic songs of male mice. PLoS Biol 2005;3:2177-2186.
  24. Jakupovic J, Kang N, Baum MJ. Effect of bilateral accessory olfactory bulb lesions on volatile urinary odor discrimination and investigation as well as mating behavior in male mice. Physiol Behav 2008;93:467-473. [PubMed: 17991495]
  25. Jamain S, Radyushkin K, Hammerschmidt K, Granon S, Boretius S, Varagueaux F, Ramanantsoa N, Gallego J, Ronnenberg A, Winter D, Frahm J, Fischer J, Bourgeron T, Ehrenreich H, Brose N. Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc Natl Acad Sci USA 2008;105:1710-1715. [PubMed: 18227507]
  26. Johns JM, Noonan LR, Zimmerman LI, McMillan BA, Means LW, Walker CH, Lubin DA, Meter KE, Nelson CJ, Pedersen CA, Mason GA, Lauder JM. Chronic cocaine treatment alters social/ aggressive behavior in Sprague-Dawley rat dams and their prenatally exposed offspring. Ann NY Acad Sci 1998;846:399-404. [PubMed: 9668435]
  27. Keverne EB. Importance of olfactory and vomernasal systems for male sexual function. Physiol Behav 2004;83:177-187. [PubMed: 15488538]
  28. Kolunie JM, Stern JM. Maternal aggression: disruption by perioral anesthesia in lactating Long-Evans rats (Rattus norvegicus). J Comp Psychol 1990;104:352-360. [PubMed: 2282784]
  29. Kwon CH, Luikart BW, Powell CM, Zhou J, Matheny SA, Zhang W, Li Y, Baker SJ, Parada LF. Pten regulates neuronal arborization and social interaction in mice. Neuron 2006;50:377-388. [PubMed: 16675393]
  30. Lainhart JE, Piven J. Diagnosis, treatment, and neurobiology of autism in children. Curr Opin Pediatr 1995;7:392-400. [PubMed: 7581642]
  31. Lin DY, Zhang S-Z, Block E, Katz LC. Encoding social signals in the mouse main olfactory bulb. Nature 2005;434:470-477. [PubMed: 15724148]
  32. Liu W, Pappas GD, Carter CS. Oxytocin receptors in brain cortical regions are reduced in haploinsufficient (+/-) reeler mice. Neurol Res 2005;27:339-345. [PubMed: 15949229]
  33. Moy SS, Nadler JJ, Magnuson TR, Crawley JN. Mouse models of autism spectrum disorders: the challenge for behavioral genetics. Med Genet 2006;142:40-51.
  34. Moy SS, Nadler JJ, Young NB, Perez A, Holloway LP, Barbaro RP, Barbaro JR, Wilson LM, Threadgill DW, Lauder JM, Magnuson TR, Crawley JN. Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav Brain Res 2007;176:4-20. [PubMed: 16971002]
  35. Mucignat-Caretta C, Bondi M, Caretta A. Time course of alterations after olfactory bulbectomy in mice. Physiol Behav 2006;89:637-643. [PubMed: 16973183]
  36. Nadler JJ, Moy SS, Dold G, Trang D, Simmons N, Perez A, Young NB, Barbaro RP, Piven J, Magnuson TR, Crawley JN. Automated apparatus for quantification of social approach behaviors in mice. Genes Brain Behav 2004;3:303-314. [PubMed: 15344923]
  37. Neckers LM, Zarrow MX, Myers MM, Denenberg VH. Influence of olfactory bulbectomy and the serotonergic system upon intermale aggression and maternal behavior in the mouse. Pharmacol Biochem Behav 1975;3:545-550. [PubMed: 242012]
  38. Nicolas LB, Prinssen EP. Social approach-avoidance behavior of a high-anxiety strain of rats: effects of benzodiazepine receptor ligands. Psychopharmacology 2006;184:65-74. [PubMed: 16328377]
  39. Otmakova NA, Gurevich EV, Katkov YA, Nesterova IV, Bobkova NV. Dissociation of multiple behavioral effects between olfactory bulbectomized C57Bl/6J and DBA/2J mice. Physiol Behav 1992;52:441-448. [PubMed: 1409903]
  40. Panksepp JB, Lahvis GP. Social reward among juvenile mice. Genes Brain Behav 2007;6:661-671. [PubMed: 17212648]
  41. Pellis SM, McKenna MM, Field EF, Pellis VC, Prusky GT, Whishaw IQ. Use of vision by rats in play fighing and other close-quarter social interactions. Physiol Behav 1996;59:905-913. [PubMed: 8778885]
  42. Portfors CV. Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci 2007;46:28-34. [PubMed: 17203913]
  43. Restrepo D, Arellano J, Oliva AM, Schaefer ML, Lin W. Emerging views of the distinct but related roles of the main and accessory olfactory systems in responsiveness to chemosensory signals in mice. Horm Behav 2004;46:247-256. [PubMed: 15325226]
  44. Ricceri L, Moles A, Crawley J. Behavioral phenotyping of mouse models of neurodevelopmental disorders: relevant social behavior patterns across the life span. Behav Brain Res 2007;176:40-52. [PubMed: 16996147]
  45. Rustay NR, Wrenn CC, Kinney JW, Holmes A, Bailey KR, Sullivan TL, Harris AP, Long KC, Saavedra MC, Starosta G, Innerfield CE, Yang RJ, Dreiling JL, Crawley JN. Galanin impairs performance on learning and memory tasks: findings from galanin transgenic and GAL-R1 knockout mice. Neuropeptides 2005;39:239-243. [PubMed: 15944016]
  46. Sanchez-Andrande G, James BM, Kendrick KM. Neural encoding of olfactory recognition memory. J Reprod Dev 2005;51:547-558. [PubMed: 16284449]
  47. Schaefer ML, Yamazaki K, Osada K, Restrepo D, Beauchamp GK. Olfactory fingerprints for major histocompatibility complex determined body odors II: relationship among odor maps, genetics, odor composition, and behavior. J Neurosci 2002;22:9513-9521. [PubMed: 12417675]
  48. Schaefer ML, Young DA, Restrepo D. Olfactory fingerprints for major histocompatibility complex- determined body odors. J Neurosci 2001;21:2481-2487. [PubMed: 11264322]
  49. Shair HN. Acquisition and expression of a socially mediated separation response. Behav Brain Res 2007;182:180-192. [PubMed: 17379325]
  50. Strasser S, Dixon AK. Effects of visual and acoustic deprivation on agonistic behaviour of the albino mouse (M. musculus L.). Physiol Behav 1986;36:773-778. [PubMed: 3714851]
  51. Valsecchi P, Galef BG Jr. Social influences on the food preference of house mice (Mus musculus). Int J Comp Psychol 1989;2:245-256.
  52. Wersinger SR, Temple JL, Caldwell HK, Young WS 3rd. Inactivation of the oxytocin and the vasopressin (Avp) 1b receptor genes, but not the Avp 1a receptor gene, differentially impairs the Bruce effect in laboratory mice (Mus musculus). Endocrinology 2008;149:116-121. [PubMed: 17947352]
  53. Wrenn CC, Harris AP, Saavedra MC, Crawley JN. Social transmission of food preference in mice: methodology and application to galanin-overexpressing transgenic mice. Behav Neurosci 2003;117:21-31. [PubMed: 12619904]
  54. Yang M, Scattoni ML, Zhodzishsky V, Chen T, Caldwell H, Young WS, McFarlane HG, Crawley JN. Social approach behaviors are similar on conventional versus reverse lighting cycles, and in replications across cohorts, in BTBR + tf/J, C57BL/6J, and vasopressin receptor 1B mutant mice. Front Behav Neurosci 2007;1:1-9. [PubMed: 18958184]
  55. Yang M, Zhodizishsky V, Crawley JN. Social deficits in BTBR T+tf/J mice are unchanged by cross- fostering with C57BL/6J mothers. Int J Dev Neurosci 2007;25:515-521. [PubMed: 17980995]
  56. Young LJ, Pitkow LJ, Ferguson JN. Neuropeptides and social behavior: animal models relevant to autism. Mol Psychiatry 2002;7:S38-S39. [PubMed: 12142945]

Cited by

Sorted by citations

Authors
Ryan, B. C., Young, N. B., Moy, S. S., & Crawley, J. N.
Affiliations
University of North Carolina at Chapel Hill (US)
Corresponding author
Ryan, Bryce C.
Venue
Behavioural Brain Research
Publisher
Elsevier BV
Published
2008-11
Volume
193
Issue
2
Pages
235-242
ISSN
0166-4328 (ISSN-L)
OpenAlex
W2032781065
Cited by
95
References
9
Citations by year
2026: 9 · 2025: 3 · 2024: 6 · 2023: 7 · 2022: 4 · 2021: 5 · 2020: 3 · 2019: 3 · 2018: 4 · 2017: 1 · 2016: 6 · 2015: 7 · 2014: 5 · 2013: 9 · 2012: 5
FWCI
3.11
Type
journal article
Language
en
Open access
Locations
  • Behavioural Brain Research (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
  • UNC Libraries
Funders
  • National Institute for Health and Care Research
  • National Institutes of Health
  • University of North Carolina at Chapel Hill
  • National Institute of Mental Health (HD40127)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32-HD-40127, P30-HD03110, P30HD003110, T32HD040127)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords
olfactory cues, social approach behavior, social transmission of food preference, autism-like behavior, mouse models of autism, sociability, social investigation, sensory cues, C57BL/6J mice
MeSH terms
Animals, Animal Communication, Autistic Disorder, Behavior, Animal, Biological Assay, Cues, Disease Models, Animal, Exploratory Behavior, Food Preferences, Male, Mice, Inbred C57BL, Social Behavior, Recognition, Psychology, Mice

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