Beating the boojum: Comparative approaches to the neurobiology of social behavior

Neuropharmacology

Volumn 58, Issue 1, 2010, Pages 17-28

  Phelps, Steven M ^a   Campbell, Polly ^a   Zheng, Da Jiang ^a   Ophir, Alexander G ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Autism; avpr1a; Ecology; Evolution; Exotic model systems; Hippocampus; Mating system; Microtus; Nucleus accumbens; OTR; Oxtr; Oxytocin; Pairbonding; Posterior cingulate cortex; Retrosplenial cortex; Schizophrenia; Scotinomys; Singing mice; Social behavior; Spatial memory; V1aR; Vasopressin; Ventral pallidum; Vocalization

Indexed keywords

NEUROPEPTIDE; OXYTOCIN; OXYTOCIN RECEPTOR; VASOPRESSIN; VASOPRESSIN V1A RECEPTOR;

ANIMAL COMMUNICATION; ARTICLE; EPISODIC MEMORY; GENE EXPRESSION REGULATION; GLOBUS PALLIDUS; HIPPOCAMPUS; HORMONAL REGULATION; INTRASPECIFIC VARIATION; NERVE CELL NETWORK; NEUROBIOLOGY; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; REGULATORY SEQUENCE; REPRODUCTIVE SUCCESS; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SPATIAL MEMORY; SPECIES DIFFERENCE; VERBAL COMMUNICATION; VOCALIZATION;

ANIMALS; BRAIN; BRAIN MAPPING; HUMANS; NEUROBIOLOGY; NEUROPEPTIDES; OXYTOCIN; SEX FACTORS; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SPECIES SPECIFICITY; VASOPRESSINS;

EID: 71549142550     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2009.06.043     Document Type: Article

References (93)

1. American Psychiatric Association, 2000. Diagnostic and Statistical Manual of Mental Disorders (4th, text revision (DSM-IV-TR) ed.).
2. Aragona B.J., Liu Y., Yu Y.J., Curtis J.T., Detwiler J.M., Insel T.R., and Wang Z.X. Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nature Neuroscience 9 (2006) 133-139
3. Ashkenazy T., Einat H., and Kronfeld-Schorr N. We are in the dark here: induction of depression- and anxiety-like behaviours in the diurnal fat sand rat, by short daylight or melatonin injections. International Journal of Neuropsychopharmacology 12 (2009) 83-93
4. Askland K., Read C., and Moore J. Pathways-based analyses of whole-genome association study data in bipolar disorder reveal genes mediating ion channel activity and synaptic neurotransmission. Human Genetics 125 (2009) 63-79
5. Bachner-Melman, R., Dina, C., Zohar, A.H., Constantini, N., Lerer, E., Hoch, S., Sella, S., Nemanov, L., Gritsenko, I., Lichtenberg, P., Granot, R., Ebstein, R.P., 2005. AVPR1a and SLC6A4 gene polymorphisms are associated with creative dance performance. PLoS Genetics 1:e42.
6. Bartz J.A., and Hollander E. The neuroscience of affiliation: forging links between basic and clinical research on neuropeptides and social behavior. Hormones and Behavior 50 (2006) 518-520
7. Beach F.A. The snark was a boojum. American Psychologist 5 (1950) 115-124
8. Beery A.K., Lacey E.A., and Francis D.D. Oxytocin and vasopressin receptor distributions in a solitary and a social species to tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). Journal of Comparative Neurology 507 (2008) 1847-1859
9. Campbell P., Ophir A.G., and Phelps S.M. Central vasopressin and oxytocin receptor distributions in two species of singing mice. Journal of Comparative Neurology 516 (2009) 321-333
10. Carroll L. The Hunting of the Snark, an Agony in Eight Fits (1898), Macmillan Company, New York
11. Carter C.S. Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders?. Behavioral Brain Research 176 (2007) 170-186
12. Cichon S., Craddock N., Daly M., Faraone S.V., Gejman P.V., Kelsoe J., Lehner T., Levinson D.F., Moran A., Sklar P., and Sullivan P.F. Genomewide association studies: history, rationale, and prospects for psychiatric disorders. American Journal of Psychiatry 166 (2009) 540-556
13. Clark A.G., Eisen M.B., Smith D.R., et al. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450 (2007) 203-218 (100 author paper)
14. Cook E.H., and Scherer S.W. Copy-number variations associated with neuropsychiatric conditions. Nature 455 (2008) 919-993
15. Cooper B.G., Manka T.F., and Mizumori S.J.Z. Finding your way in the dark: the retrosplenial cortex contributes to spatial memory and navigation without visual cues. Behavioral Neuroscience 115 (2001) 1012-1028
16. Crino, A., 2008. Divergent Stress Coping Styles and Singing Behavior in the Short-tailed Singing Mouse (Scotinomys teguina). Master's thesis. University of Florida.
17. Donaldson Z.R., Kondrashov F.A., Putnam A., Bai Y., Stoinski T.L., Hammock E.A., and Young L.J. Evolution of a behavior-linked microsatellite-containing element in the 5' flanking region of the primate AVPR1A gene. BMC Evolutionary Biology 8 (2008) 180
18. DeLong E.F., Preston C.M., Mincer T., et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 311 (2006) 496-503 (12 author paper)
19. Ebensperger L.A. A review of the evolutionary causes of rodent group-living. Acta Theriologica 46 (2001) 115-144
20. Fink G.R., Markowitsch H.J., Reinkemeier M., Bruckbauer T., Kessler J., and Heiss W.D. Cerebral representation of one's own past: neural networks involved in autobiographical memory. Journal of Neuroscience 16 (1996) 4275-4282
21. Fink S., Excoffier L., and Heckel G. Mammalian monogamy is not controlled by a single gene. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 10956-10960
22. Fisher S.E., Lai C.S.L., and Monaco A.P. Deciphering the genetic basis of speech and language disorders. Annual Review of Neuroscience 26 (2003) 57-80
23. Felsenstein J. Phylogenetics and the comparative method. American Naturalist 125 (1985) 1-15
24. Gervais H., Belin P., Boddaert N., Leboyer M., Coez M., Sfaello I., Barthelemy C., Brunelle F., Samson Y., and Zilbovicius M. Abnormal cortical voice processing in autism. Nature Neuroscience 7 (2004) 801-802
25. Getz L.L., Carter C.S., and Gavish L. The mating system of the prairie vole, Microtus ochrogaster - field and laboratory evidence for pair-bonding. Behavioral Ecology and Sociobiology 8 (1981) 189-194
26. Getz L.L., McGuire B., Pizzuto T., Hofmann J.E., and Frase B. Social-organization of the prairie vole (Microtus ochrogaster). Journal of Mammalogy 74 (1993) 44-58
27. Goodson J.L., and Bass A.H. Social behavior function and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Research Reviews 35 (2001) 246-255
28. Goodson J.L., Evans A.K., and Bass A.H. Putative isotocin distributions in sonic fish: relation to vasotocin and vocal-acoustic circuitry. Journal of Comparative Neurology 462 (2003) 1-14
29. Hammock E.A.D., Lim M.M., Nair H.P., and Young L.J. Association of vasopressin 1a receptor levels with a regulatory microsatellite and behavior. Genes, Brain and Behavior 4 (2005) 289-301
30. Hammock E.A.D., and Young L.J. Functional microsatellite polymorphism associated with divergent social structure in vole species. Molecular Biology and Evolution 21 (2004) 1057-1063
31. Hammock E.A.D., and Young L.J. Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308 (2005) 1630-1634
32. Harker K.T., and Whishaw I.Q. A reaffirmation of the retrosplenial contribution to rodent navigation: reviewing the influences of lesion, strain, and task. Neuroscience and Biobehavioral Reviews 28 (2004) 485-496
33. Harrison P.J. The neuropathology of schizophrenia. Brain 122 (1999) 593-624
34. Heckers S., Rauch S.L., Goff D., Savage C.R., Schacter D.L., Fischman A.J., and Alpert N.M. Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nature Neuroscience 4 (1998) 318-323
35. Hooper, E.T., 1972. A Synopsis of the Rodent Genus Scotinomys. Occasional Papers of the Museum of Zoology, University of Michigan 665, pp. 1-32.
36. Hooper E.T., and Carleton M.D. Reproduction, Growth and Development in Two Contiguously Allopatric Rodent Species, Genus Scotinomys (1976), Miscellaneous Publications, Museum of Zoology, University of Michigan 151 pp. 1-52
37. Insel T.R. A neurobiological basis of social attachment. American Journal of Psychiatry 154 (1997) 726-735
38. Insel, T.R., Gelhard, R., Shapiro, L.E., 1991. The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice. Neuroscience 43, 623-630.
39. Insel T.R., and Shapiro L.E. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proceedings of the National Academy of Sciences of the United States of America 89 (1992) 5981-5985
40. Insel T.R., Wang Z.X., and Ferris C.F. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. Journal of Neuroscience 14 (1994) 5381-5392
41. Jansa S.A., and Weksler M. Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Molecular Phylogenetics and Evolution 31 (2004) 256-276
42. Jacob S., Brune C.W., Carter C.S., Leventhal B.L., Lord C., and Cook Jr. E.H. Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism. Neuroscience Letters 417 (2007) 6-9
43. Kim S.J., Young L.J., Gonen D., Veenstra-VanderWeele J., Courchesne R., Courchesne E., Lord C., Leventhal B.L., Cook E.H., and Insel T.R. Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Molecular Psychiatry 7 (2002) 503-507
44. Kinsley C.H., and Lambert K.G. Reproduction-induced neuroplasticity: natural behavioural and neuronal alterations associated with the production and care of offspring. Journal of Neuroendocrinology 20 (2008) 515-525
45. Kirsch P., Esslinger C., Chen Q., Mier D., Lis S., Siddhanti S., Gruppe H., Mattay V.S., Gallhofer B., and Meyer-Lindenberg A. Oxytocin modulates neural circuitry for social cognition and fear in humans. Journal of Neuroscience 25 (2005) 11489-11493
46. Kokko H. Cuckoldry and the stability of biparental care. Ecology Letters 2 (1999) 247-255
47. Knafo A., Israel S., Darvasi A., Bachner-Melman R., Uzefovsky F., Cohen L., Feldman E., Lerer E., Laiba E., Raz Y., Nemanov L., Gritsenko I., Dina C., Agam G., Dean B., Bornstein G., and Ebstein R.P. Individual differences in allocation of funds in the dictator game associated with length of the arginine vasopressin 1a receptor RS3 promoter region and correlation between RS3 length and hippocampal mRNA. Genes, Brain and Behavior 7 (2008) 266-275
48. Kokko H., and Jennions M.D. Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology 21 (2008) 919-948
49. Kokko H., and Morrell L.J. Mate guarding, male attractiveness, and paternity under social monogamy. Behavioral Ecology 16 (2005) 724-731
50. Komers P.E., and Brotherton P.N.M. Female space use is the best predictor of monogamy in mammals. Proceedings of the Royal Society of London Series B 264 (1997) 1261-1270
51. Korff S., Stein D.J., and Harvey B.H. Stereotypic behaviour in the deer mouse: pharmacological validation and relevance for obsessive compulsive disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 32 (2008) 348-355
52. Lerer E., Levi S., Salomon S., Darvasi A., Yirmiya N., and Ebstein R.P. Association between the oxytocin receptor (OXTR) gene and autism: relationship to Vineland adaptive behavior scales and cognition. Molecular Psychiatry 13 (2008) 980-988
53. Lewis M.H., Tanimura Y., Lee L.W., and Bodfish J.W. Animal models of restricted repetitive behavior in autism. Behavioural Brain Research 176 (2007) 66-74
54. Levin R., Heresco-Levy U., Bachner-Melman R., Israel S., Shalev I., and Ebstein R.P. Association between arginine vasopressin 1a receptor (AVPR1a) promoter region polymorphisms and prepulse inhibition. Psychoneuroendocrinology 34 (2009) 901-908
55. Lim M.M., Wang Z., Olazabal D.E., Ren X., Terwilliger E.F., and Young L.J. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429 (2004) 754-757
56. Lim M.M., and Young L.J. Vasopressin-dependent neural circuits underlying pair bonding in the monogamous prairie vole. Neuroscience 125 (2004) 35-45
57. Lim M.M., Bielsky I.F., and Young L.J. Neuropeptides and the social brain: potential rodent models of autism. International Journal of Developmental Neuroscience 23 (2005) 235-243
58. Liu, Y., Curtis, J.T., Wang, Z.-X., 2001. Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). Behavioral Neuroscience 155, 910-919.
59. Lord C., Leventhal B.L., and Cook E.H. Quantifying the phenotype in autism spectrum disorders. American Journal of Medical Genetics 105 (2001) 36-38
60. Maguire E.A. The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scandinavian Journal of Psychology 42 (2001) 225-238
61. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Review of Neuroscience 24 (2001) 1161-1192
62. Miller J.R., and Engstrom M.D. Vocal stereotypy and singing behavior in Baiomyine mice. Journal of Mammalogy 88 (2007) 1447-1465
63. Muller R.A., Behen M.E., Rothermel R.D., Chugani D.C., Muzik O., Mangner T.J., and Chugani H.T. Brain mapping of language and auditory perception in high-functioning autistic adults: a PET study. Journal of Autism and Developmental Disorders 29 (1999) 19-31
64. Ophir A.G., Campbell P., Hanna K., and Phelps S.M. Field tests of cis-regulatory variation at the prairie vole avpr1a locus: association with V1aR abundance but not sexual or social fidelity. Hormones and Behavior 54 (2008) 694-702
65. Ophir A.G., Sorin A.B., Phelps S.M., and Wolff J.O. Social but not genetic monogamy is associated with greater breeding success in prairie voles. Animal Behaviour 75 (2008) 1143-1154
66. Ophir A.G., Wolff J.O., and Phelps S.M. Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings. Proceedings of the National Academy of Sciences of the United States of America 105 (2008) 1249-1254
67. Ophir, A.G., Zheng, D-J, Eans, S., Phelps, S.M., 2009. Social investigation in a memory task relates to neural variation in oxytocin receptor but not vasopressin receptor 1a. Behavioral Neuroscience, in press.
68. 8-vasopressin in the Hebb-Williams maze. Behavioural Brain Research 141 (2003) 1-9
69. Phelps, S.M., Ophir, A.G. Monogamous brains and alternative tactics: neuronal V1aR, space use and sexual infidelity among male prairie voles. In: Reuven Dukas (Ed.), Cognitive Ecology, 2nd edn. University of Chicago Press, in press.
70. Phelps S.M., and Young L.J. Extraordinary diversity in vasopressin (v1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation. Journal of Comparative Neurology 466 (2003) 564-576
71. Pitkow L.J., Sharer C.A., Ren X.H., Insel T.R., Terwilliger E.F., and Young L.J. Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. Journal of Neuroscience 21 (2001) 7392-7396
72. Ross H.E., Freeman S.M., Spiegel L.L., Ren X.H., Terwilliger E.F., and Young L.J. Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. Journal of Neuroscience 29 (2009) 1312-1318
73. Rosso L., Keller L., Kaessmann H., and Hammond R.L. Mating system and avpr1a promoter variation in primates. Biology Letters 4 (2008) 375-378
74. Sandell M., and Liberg O. Roamers and stayers - a model on male mating tactics and mating systems. American Naturalist 139 (1992) 177-189
75. Solomon N.G., and Jacquot J.J. Characteristics of resident and wandering prairie voles, Microtus ochrogaster. Canadian Journal of Zoology 80 (2002) 951-955
76. Smeltzer M.D., Curtis J.T., Aragona B.J., and Wang Z.X. Dopamine, oxytocin, and vasopressin receptor binding in the medial prefrontal cortex of monogamous and promiscuous voles. Neuroscience Letters 394 (2006) 146-151
77. Stefansson H., Rujescu D., Cichon S., et al. Large recurrent microdeletions associated with Schizophrenia. Nature 455 (2008) 178-179 (75 author paper)
78. Steppan S.J., Adkins R.M., and Anderson J. Phylogeny and divergence-data estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology 53 (2004) 533-553
79. Swaab D.F., Bao A.M., and Lucassen P.J. The stress system in the human brain in depression and neurodegeneration. Ageing Research Reviews 4 (2005) 141-194
80. Szatmari P., Paterson A.D., Zwaigenbaum L., et al. Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nature Genetics 39 (2007) 319-328 (137 author paper)
81. Tanguay P.E., Robertson J., and Derrick A. A dimensional classification of autism spectrum disorder by social communication domains. Journal of the American Academy of Child and Adolescent Psychiatry 37 (1998) 271-277
82. Thibonnier M., Graves M.K., Wagner M.S., Chatelain N., Soubrier F., Corvol P., Willard H.F., and Jeunemaitre X. Study of V-1-vascular vasopressin receptor gene microsatellite polymorphisms in human essential hypertension. Journal of Molecular and Cellular Cardiology 32 (2000) 557-564
83. Tomizawa K., Iga N., Lu Y.-F., Moriwaki A., Matsushita M., Li S.-T., Miyamoto O., Itano T., and Matsui H. Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade. Nature Neuroscience 6 (2003) 384-390
84. van Wimersma Greidanus Tj.B., and Maigret C. The role of limbic vasopressin and oxytocin in social recognition. Brain Research 713 (1996) 153-159
85. Walum H., Westberg L., Henningsson S., Neiderhiser J.M., Reiss D., Igl W., Ganiban J.M., Spotts E.L., Pedersen N.L., Eriksson E., and Lichtenstein P. Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proceedings of the National Academy of Sciences 105 (2008) 14153-14156
86. Wang Z.X., Ferris C.F., and DeVries G.J. Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proceedings of the National Academy of Sciences of the United States of America 91 (1994) 400-404
87. Winslow, J.T., Hastings, N., Carter, C.S., Harbaugh, C.R., Insel, T.R., 1993. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365, 545-548.
88. Winslow J.T., and Insel T.R. The social deficits of the oxytocin knockout mouse. Neuropeptides 36 (2002) 221-229
89. Wu S.P., Jia M.X., Ruan Y., Liu J., Guo Y.Q., Shuang M., Gong X.H., Zhang Y.B., Yang X.L., and Zhang D. Positive association of the oxytocin receptor gene (OXTR) with autism in the Chinese Han population. Biological Psychiatry 58 (2005) 74-77
90. Yirmiya N., Rosenberg C., Levi S., Salomon S., Shulman C., Nemanov L., Dina C., and Ebstein R.P. Association between the arginine vasopressin 1a receptor (AVPR1a) gene and autism in a family-based study: mediation by socialization skills. Molecular Psychiatry 11 (2006) 488-494
91. Young L.J., Lim M.M., Gingrich B., and Insel T.R. Cellular mechanisms of social attachment. Hormones and Behavior 40 (2001) 133-138
92. Young L.J., Nilsen R., Waymire K.G., MacGregor G.R., and Insel T.R. Increased affiliative response to vasopressin in mice expressing the v-1a receptor from a monogamous vole. Nature 400 (1999) 766-768
93. Young L.J., and Wang Z. The neurobiology of pairbonding. Nature Neuroscience 7 (2004) 1048-1054