Sociability and preference for social novelty in five inbred strains: An approach to assess autistic-like behavior in mice

Genes, Brain and Behavior

Volumn 3, Issue 5, 2004, Pages 287-302

  Moy, S S ^a   Nadler, J J ^a   Perez, A ^a   Barbaro, R P ^a   Johns, J M ^a   Magnuson, T R ^a   Piven, J ^a   Crawley, J N ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Autism; Exploration; Inbred strains; Locomotion; Mice; Olfaction; Rotarod; Sociability; Social interaction; Social preference

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUTISM; FEMALE; INBRED STRAIN; LOCOMOTION; MALE; MOTOR COORDINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMELLING; SOCIAL BEHAVIOR; SOCIAL INTERACTION; TASK PERFORMANCE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; AUTISTIC DISORDER; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; FEMALE; LOCOMOTION; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, INBRED STRAINS; REPRODUCIBILITY OF RESULTS; ROTAROD PERFORMANCE TEST; SEX FACTORS; SOCIAL BEHAVIOR; SPECIES SPECIFICITY;

ANIMALIA;

EID: 4644373224     PISSN: 16011848     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1601-1848.2004.00076.x     Document Type: Article

References (73)

1. American Psychiatric Association (1994) Diagnostic and Statistical Manual of Mental Disorders (DSM-IV). American Psychiatric Association, Washington, DC.
2. Bachevalier, J. (1991) An animal model for childhood autism: memory loss and socioemotion disturbances following neonatal damage to the limbic system in monkeys. In Tamminga, C. A. & Shulz, S. C. (eds), Advances in Neuropsychiatry and Psychopharmacology. Raven Press, Ltd, New York, pp. 129-140.
3. Bailey, A., Le Couteur, A., Gottesman, I., Bolton, P., Simonoff, E., Yuzda, E. & Rutter, M. (1995) Autism as a strongly genetic disorder: evidence from a British twin study. Psychol Med 25, 63-77.
4. Bakker, C. E., Verheij, C., Willemsen, R., van der Helm, R., Oerlemans, F., Vermey, M., Bygrave, A., Hoogeveen, A.T., Oostra, B.A., Reyniers, E., De Boulle, K., D'Hooge, R., Cras, P., van Velzen, D., Nagels, G., Martin, J.-J., De Deyn, P.P., Darby, J.K. & Willems, P.J. (1994) Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 78, 23-33.
5. Bales, K.L. & Carter, C.S. (2003) Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster). Behav Neurosci 17, 854-859.
6. Baranek, G.T. (2002) Efficacy of sensory and motor interventions for children with autism. J Autism Dev Disorders 32, 397-422.
7. Barrett, S., Beck, J.C., Bernier, R., Bisson, E., Braun, T.A., Casavant, T.L., Childress, D., Folstein, S.E., Garcia, M., Gardiner, M.B., Gilman, S., Haines, J.L., Hopkins, K., Landa, R., Meyer, N.H., Mullane, J.A., Nishimura, D.Y., Palmer, P., Piven, J., Purdy, J., Santangelo, S.L., Searby, C., Sheffield, V., Singleton, J., Slager, S., Struchen, T., Svenson, S., Vieland, V., Wang, K. & Winklosky, B. (1999) An autosomal genomic screen for autism. Collaborative linkage study of autism. Am J Med Genet (Neuropsych) 88, 609-615.
8. Bauman, M. & Kemper, T.L. (1985) Histoanatomic observations of the brain in early infantile autism. Neurology 35, 866-874.
9. Blanchard, D.C., Griebel, G. & Blanchard, R.J. (2003) The mouse defense test battery: pharmacological and behavioral assays for anxiety and panic. Eur J Pharmacol 28, 97-116.
10. Bluthe, R.M., Gheusi, G. & Dantzer, R. (1993) Gonadal steroids influence the involvement of arginine vasopressin in social recognition in mice. Psychoneuroendocrinology 18, 323-335.
11. Bodfish, J.W., Symons, F.J., Parker, D.E. & Lewis, M. (2000) Varieties of repetitive behavior in autism: comparisons to mental retardation. J Autism Dev Disorders 30, 237-243.
12. Bouwknecht, J.A. & Paylor, R. (2002) Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Behav Brain Res 136, 489-501.
13. Brodkin, E.S., Hagemann, A., Nemetski, S.M. & Silver, L.M. (2004) Social approach-avoidance behavior of inbred mouse strains towards DBA/2 mice. Brain Res 1002, 151-157.
14. Carter, S.A., DeVries, A.C. & Getz, L.L. (1995) Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci Biobehav Rev 19, 303-314.
15. Cheal, M.L. & Sprott, R.L. (1971) Social olfaction: a review of the role of olfaction in a variety of animal behaviors. Psychol Rep 29, 195-243.
16. Chen, L. & Toth, M. (2001) Fragile X mice develop sensory hyperreactivity to auditory stimuli. Neurosci 103, 1043-1050.
17. Churchill, J.D., Grossman, A.W., Irwin, S.A., Galvez, R., Klintsova, A.Y., Weiler, I.J. & Greenough, W.T. (2002) A converging-methods approach to fragile X syndrome. Dev Psychobiol 40, 323-338.
18. Crawley, J.N. (2000) What's Wrong with My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice. John Wiley & Sons, Inc, New York.
19. Dluzen, D.E. & Kreutzberg, J.D. (1993) 1-Methyl-4-phenyl-1,2,3,6- tetrahydropyridine (MPTP) disrupts social memory/recognition processes in the male mouse. Brain Res 609, 98-102.
20. Dobkin, C., Rabe, A., Dumas, R., El Idrissi, A., Haubenstock, H. & Brown, W.T. (2000) Fmr1 knockout mouse has a distinctive strain-specific learning impairment. Neurosci 100, 423-429.
21. Ferguson, J.N., Young, L.J., Hearn, E.F., Matzuk, M.M., Insel, T.R. & Winslow, J.T. (2000) Social amnesia in mice lacking the oxytocin gene. Nature Genet 25, 284-288.
22. File, S.E. & Seth, P. (2003) A review of 25 years of the social interaction test. Eur J Pharmacol 463, 35-53.
23. Folstein, S.E. & Rosen-Sheidley, B. (2001) Genetics of autism: complex aetiology for a heterogeneous disorder. Nature Rev/Genetics 2, 943-955.
24. Fombonne, E. (2003) Epidemiological surveys of autism and other pervasive developmental disorders: an update. J Aut Dev Disorders 33, 365-382.
25. Gheusi, G., Bluthe, R.M., Goodall, G. & Dantzer, R. (1994) Social and individual recognition in rodents: Methodological aspects and neurobiological bases. Behav Processes 33, 59-88.
26. Grant, E.C. & MacIntosh, J.H. (1963) A comparison of the social postures of some common laboratory rodents. Behaviour 21, 246-259.
27. Hagerman, R.J., Jackson, A.W. III, Levitas, A., Rimland, B. & Braden, M. (1986) An analysis of autism in fifty males with the fragile X syndrome. Am J Med Genet 23, 359-374.
28. Hallett, M., Lebiedowska, M.K., Thomas, S.L., Stanhope, S.J., Denckla, M.B. & Rumsey, J. (1993) Locomotion of autistic adults. Arch Neurol 50, 1304-1308.
29. Happé, F., Ehlers, S., Fletcher, P., Frith, U., Johansson, M., Gillberg, C., Dolan, R., Frackowiak, R. & Frith, C. (1996) 'Theory of mind' in the brain. Evidence from a PET scan study of Asperger syndrome. Neuroreport 8, 197-201.
30. Holmes, A., Kinney, J.W., Wrenn, C.C., Li, Q., Yang, R.J., Ma, L., Vishwanath, J., Saavedra, M.C., Innerfield, C.E., Jacoby, A.S., Shine, J., Iismaa, T.P. & Crawley, J.N. (2003) Galanin GAL-R1 receptor null mutant mice display increased anxiety-like behavior specific to the elevated plus-maze. Neuropsychopharm 28, 1031-1044.
31. Insel, T.R. (2001) Mouse models for autism: report from a meeting. Mammalian Genome 12, 755-757.
32. Insel, T.R. & Young, L.J. (2001) The neurobiology of attachment. Nat Rev Neurosci 2, 129-136.
33. Kanner, L. (1943) Autistic disturbances of affective contact. Nervous Child 2, 217-250.
34. Kanner, L. (1973) The birth of early infantile autism. J Autism Child Schizophrenia 3, 93-95.
35. Kogan, J.H., Frankland, P.W. & Silva, A.J. (2000) Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10, 47-56.
36. Laviola, J. & Terranova, M.L. (1998) The developmental psychobiology of behavioural plasticity in mice: the role of social experiences in the family unit. Neurosci Biobehav Rev 23, 197-213.
37. Liebenaur, L.L. & Slotnick, B.M. (1996) Social organization and aggression in a group of olfactory bulbectomized male mice. Physiol Behav 60, 403-409.
38. Lijam, N., Paylor, R., McDonald, M.P., Crawley, J.N., Deng, C.-X., Herrup, K., Stevens, K.E., Maccaferri, G., McBain, C.J., Sussman, D.J. & Wynshaw-Boris, A. (1997) Social interaction and sensorimotor gating abnormalities in mice lacking. Dvl1 Cell 90, 895-905.
39. Lord, C., Cook, E.H., Leventhal, B.L. & Amaral, D.G. (2000a) Autism spectrum disorders. Neuron 28, 355-363.
40. Lord, C., Risi, S., Lambrecht, L., Cook, E.H. Jr., Leventhal, B.L., DiLavore, P.C., Pickles, A. & Rutter, M. (2000b) The Autism Diagnostic Observation Schedule-Generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disorders 30, 205-223.
41. Mathis, C., Neumann, P.E., Gershenfeld, H., Paul, S.M. & Crawley, J.N. (1995) Genetic analysis of anxiety-related behaviors and responses to benzodiazepine-related drugs in AXB and BXA recombinant inbred mouse strains. Behav Genet 25, 557-568.
42. Mathis, C., Paul, S.M. & Crawley, J.N. (1994) Characterization of benzodiazepine-sensitive behaviors in the A/J and the C57BL/6J inbred strains of mice. Behav Genet 24, 171-180.
43. Mineur, Y.S., Sluyter, F., de Wit, S., Oostra, B.A. & Crusio, W.E. (2002) Behavioral and neuroanatomical characterization of the Fmr1 knockout mouse. Hippocampus 12, 39-46.
44. Mohn, A.R., Gainetdinov, R.R., Caron, M.G. & Koller, B.H. (1999) Mice with reduced NMDA receptor expression display behaviors related to schizophrenia. Cell 98, 427-436.
45. Nadler, J.J., Moy, S.S., Dold, G., Trang, D., Simmons, N., Perez, A., Young, N.B., Barbaro, R.P., Piven, J., Magnuson, T.R. & Crawley, J.N. (2004) Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav 3, doi: 10.1111/j.1601-183X.2004.00071.x
46. Nielson, D.M., Derber, W.J., McClellan, D.A. & Crnic, L.S. (2002) Alterations in the auditory startle response in Fmr1 targeted mutant mouse models of fragile X syndrome. Brain Res 927, 8-17.
47. Paul, R. (2003) Promoting social communication in high functioning individuals with autism spectrum disorders. Child Adolesc Psychiatr Clin N Am 12, 87-106.
48. Peier, A.M., McIlwain, K.L., Kenneson, A., Warren, S.T., Paylor, R. & Nelson, D.L. (2000) (Over) correction of FMR1 deficiency with YAC transgenics: behavioral and physical features. Human Mol Genet 9, 1145-1159.
49. Philippe, A., Guilloud-Bataille, M., Martinez, M., Gillberg, C., Rastam, M., Sponheim, E., Coleman, M., Zappella, M., Aschauer, H., Penet, C., Feingold, J., Brice, A. & Leboyer, M. The Paris Autism Research International Sibpair Study (2002) Analysis of ten candidate genes in autism by association and linkage. Am J Med Genet (Neuropsych) 114, 125-128.
50. Piven, J. (2001) The broad autism phenotype: a complementary strategy for molecular genetic studies of autism. Am J Med Genet (Neuropsych) 105, 34-35.
51. Piven, J., Palmer, P., Landa, R., Santangelo, S. & Jacobi, D. (1997) Personality and language characteristics in parents from multiple-incidence autism families. Am J Med Genet (Neuropsych) 74, 398-411.
52. Risch, N., Spiker, D., Lotspeich, L., Nouri, N., Hinds, D., Hallmayer, J., Kalaydjieva, L., McCague, P., Dimiceli, S., Pitts, T., Nguyen, L., Yang, J., Harper, C., Thorpe, D., Vermeer, S., Young, H., Hebert, J., Lin, A., Ferguson, J., Chiotti, C., Wiese-Slater, S., Rogers, T., Salmon, B., Nicholas, P., Petersen, P.B., Pingree, C., McMahon, W., Wong, D.L., Cavalli-Sforza, L.L., Kraemer, H.C. & Myers, R.M. (1999) A genomic screen of autism: evidence for a multilocus etiology. Am J Human Genet 65, 493-507.
53. Ritvo, E.R., Jorde, L., Mason-Brothers, A., Freeman, B., Pingree, C., Jones, M.B., McMahon, W.M., Petersen, P.B., Jenson, W.R. & Mo, A. (1989) The UCLA-University of Utah epidemiologic survey of autism: recurrence risk estimates and genetic counseling. Am J Psychia 146, 1036.
54. Schloper, E. & Mesibov, G.B. (eds) (1987) Neurobiological Issues in Autism. Plenum Press, New York.
55. Schultz, R., Gauthier, I., Klin, A., Fulbright, R., Anderson, A., Volkmar, F., Skudlarski, P., Lacadie, C., Cohen, D. & Gore, J. (2000) Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Arch General Psychia 57, 331-340.
56. Scott, J.P. & Fredericson, E. (1951) The causes of fighting in mice and rats. Physiol Zool 24, 273-309.
57. Shao, Y., Wolpert, C.M., Raiford, K.L., Menold, M.M., Donnelly, S.L., Ravan, S.A., Bass, M.P., McClain, C., von Wendt, L., Vance, J.M., DeLong, R.G., Cuccaro, M.L. & Pericak-Vance, M.A. (2002) Genomic screen and follow-up analysis for autism disorders. Am J Med Genet (Neuropsych) 114, 99-105.
58. Shih, J.C. & Chen, K. (1999) MAO-A and - B gene knock-out mice exhibit distinctly different behavior. Neurobiology 7, 235-246.
59. Smith, G.W., Aubry, J.M., Dellu, F., Contarino, A., Bilezikjian, L.M., Gold, L.H., Chen, R., Marchuk, Y., Hauser, C., Bentley, C.A., Sawchenko, P.E., Koob, G.F., Vale, W. & Lee, K.-F. (1998) Corticotropin releasing factor receptor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20, 1093-1102.
60. Szatmari, P., Jones, M., Zwaigenbaum, L. & MacLean, J. (1998) Genetics of autism: overview and new directions. J Aut Dev Disorders 28, 351-368.
61. Tager-Flusberg, H., Joseph, R. & Folstein, S. (2001) Current directions in research on autism. Mental Retardation Dev Disabilities Res Rev 7, 21-29.
62. Tang, A.C., Reeb, B.C., Romeo, R.D. & McEwen, B.S. (2003) Modification of social memory, hypothalamic-pituitary-adrenal axis, and brain asymmetry by neonatal novelty exposure. J Neurosci 23, 8254-8260.
63. Thifault, S., Lalonde, R., Sanon, N. & Hamet, P. (2002) Comparisons between C57BL/6J and A/J mice in motor activity and coordination, hole-poking, and spatial learning. Brain Res Bull 58, 213-218.
64. Valzelli, L. (1973) The 'isolation syndrome' in mice. Psychopharmacologia 31, 305-320.
65. Vandenbergh, J.G. (1989) Coordination of social signals and ovarian function during sexual development. J Anim Sci 67, 1841-1847.
66. Wahlsten, D., Metten, P. & Crabbe, J.C. (2003) A rating scale for wildness and ease of handling laboratory mice: results for 21 inbred strains tested in two laboratories. Genes Brain Behav 2, 71-79.
67. Waite, K.A., Cabilio, N.R. & Vance, D.E. (2002) Choline deficiency-induced liver damage is reversible in Pemt-/- mice. J Nutrition 132, 68-71.
68. Winslow, J.T. (2003) Mouse social recognition and preference. In Crawley, J.N., Gerfen, C., McKay, R., Rogawski, M., Sibley, D.R., Skolnick, P. & Wray, W. (eds), Current Protocols in Neuroscience. John Wiley & Sons, Inc, New York, pp. 8.16.1-8.16.13.
69. Winslow, J.T. & Camacho, F. (1995) Cholinergic modulation of a decrement in social investigation following repeated contacts between mice. Psychopharmacology 121, 164-172.
70. Winslow, J.T. & Insel, T.R. (2002) The social deficits of the oxytocin knockout mouse. Neuropeptides 36, 221-229.
71. Wrenn, C.C., Harris, A.P., Saavedra, M.C. & Crawley, J.N. (2003) Social transmission of food preference in mice: Methodology and application to galanin-overexpressing transgenic mice. Behav Neurosci 117, 21-31.
72. Young, L.J., Pitkow, L.J. & Ferguson, J.N. (2002) Neuropeptides and social behavior: animal models relevant to autism. Mol Psychiatry 7, S38-S39.
73. Zhu, X., Song, J., Mar, M.-H., Edwards, L.J. & Zeisel, S.H. (2003) Phosphatidylethanolamine N-methyltransferase (PEMT) knockout mice have hepatic steatosis and abnormal hepatic choline metabolite concentrations despite ingesting a recommended dietary intake of choline. Biochem J 370, 987-993.