Vasopressin and social odor processing in the olfactory bulb and anterior olfactory nucleus

Annals of the New York Academy of Sciences

Volumn 1220, Issue 1, 2011, Pages 106-116

  Wacker, Douglas W ^a,b   Engelmann, Mario ^c   Tobin, Vicky A ^a   Meddle, Simone L ^a,d   Ludwig, Mike ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b Center for Language and Brain   (United States)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Olfaction; Social memory; Social recognition

Indexed keywords

4 AMINOBUTYRIC ACID; CALBINDIN; CALRETININ; VASOPRESSIN;

ARTICLE; ASSOCIATION; BEHAVIOR; DENDRITE; HUMAN; NERVE CELL; NONHUMAN; ODOR; OLFACTORY BULB; OLFACTORY NUCLEUS; PATHOLOGY; RECOGNITION; RESEARCH; SIGNAL TRANSDUCTION; VASOPRESSIN RELEASE;

MAMMALIA; RODENTIA;

EID: 79952458629     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2010.05885.x     Document Type: Article

References (104)

1. Ferris, C.F. et al 1986. A vasopressin antagonist can reverse dominant/subordinate behavior in hamsters. Physiol. Behav. 38: 135-138.
2. Ferris, C.F. & M. Potegal 1988. Vasopressin receptor blockade in the anterior hypothalamus suppresses aggression in hamsters. Physiol. Behav. 44: 235-239.
3. Winslow, J.T. et al 1993. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 365: 545-548.
4. Young, L.J. et al 1999. Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400: 766-768.
5. Goodson, J.L. 1998. Vasotocin and vasoactive intestinal polypeptide modulate aggression in a territorial songbird, the violet-eared waxbill (Estrildidae: Uraeginthus granatina). Gen. Comp. Endocrinol. 111: 233-244.
6. Goodson, J.L. 1998. Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm. Behav. 34: 67-77.
7. Goodson, J.L. & E. Adkins-Regan 1999. Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata). J. Neuroendocrinol. 11: 19-25.
8. Insel, T.R., Z.X. Wang & C.F. Ferris 1994. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J. Neurosci. 14: 5381-5392.
9. Hammock, E.A. & L.J. Young 2002. Variation in the vasopressin V1a receptor promoter and expression: implications for inter- and intraspecific variation in social behaviour. Eur. J. Neurosci. 16: 399-402.
10. Bachner-Melman, R. et al 2005. AVPR1a and SLC6A4 gene polymorphisms are associated with creative dance performance. PLoS Genet. 1: e42.
11. Knafo, A. et al 2008. 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 Behav. 7: 266-275.
12. Meyer-Lindenberg, A. et al 2009. Genetic variants in AVPR1A linked to autism predict amygdala activation and personality traits in healthy humans. Mol. Psychiatry 14: 968-975.
13. Walum, H. et al 2008. Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc. Natl. Acad. Sci. USA 105: 14153-14156.
14. Dantzer, R. et al 1988. Septal vasopressin modulates social memory in male rats. Brain Res. 457: 143-147.
15. Bielsky, I.F. et al 2004. Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 29: 483-493.
16. Bielsky, I.F. et al 2005. The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47: 503-513.
17. Landgraf, R. et al 2003. Viral vector-mediated gene transfer of the vole V1a vasopressin receptor in the rat septum: improved social discrimination and active social behaviour. Eur. J. Neurosci. 18: 403-411.
18. Wersinger, S.R. et al 2008. 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 149: 116-121.
19. Wersinger, S.R. et al 2004. Social motivation is reduced in vasopressin 1b receptor null mice despite normal performance in an olfactory discrimination task. Horm. Behav. 46: 638-645.
20. Tobin, V.A. et al 2010. An intrinsic vasopressin system in the olfactory bulb is involved in social recognition. Nature 464: 413-417.
21. Wacker, D.W. et al 2010. Expression of early growth response protein 1 (Egr-1) in vasopressin neurons of the rat anterior olfactory nucleus following social odour exposure. J. Physiol. 588: 4705-4717.
22. Bruce, H.M. 1959. An exteroceptive block to pregnancy in the mouse. Nature 184: 105.
23. Butenandt, A. et al 1959. Über den Sexuallockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Naturforschung 14: 283-284.
24. McClintock, M.K. 1971. Menstrual synchrony and suppression. Nature 229: 244-245.
25. Vandenbergh, J.G. 1967. Effect of the presence of a male on the sexual maturation of female mice. Endocrinology 81: 345-349.
26. Whitten, W.K. 1956. Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J. Endocrinol. 13: 399-404.
27. Shipley, M.T., M. Ennis & A.C. Puche 2008. The olfactory system. In Neuroscience in Medicine. P.M. Conn, Ed.: 611-622. Humana Press. Totowa.
28. Brennan, P.A. & K.M. Kendrick 2006. Mammalian social odours: attraction and individual recognition. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361: 2061-2078.
29. Herrick, C.J. 1924. The nucleus olfactorius anterior of the opossum. J. Comp. Neurol. 37: 317-359.
30. Haberly, L.B. & J.L. Price 1978. Association and commissural fiber systems of the olfactory cortex of the rat. I. Systems originating in the piriform cortex and adjacent areas. J. Comp. Neurol. 178: 711-740.
31. Illig, K.R. & J.D. Eudy 2009. Contralateral projections of the rat anterior olfactory nucleus. J. Comp. Neurol. 512: 115-123.
32. Mohedano-Moriano, A. et al 2005. Reciprocal connections between olfactory structures and the cortex of the rostral superior temporal sulcus in the Macaca fascicularis monkey. Eur. J. Neurosci. 22: 2503-2518.
33. Lei, H., R. Mooney & L.C. Katz 2006. Synaptic integration of olfactory information in mouse anterior olfactory nucleus. J. Neurosci. 26: 12023-12032.
34. Brunjes, P.C., K.R. Illig & E.A. Meyer 2005. A field guide to the anterior olfactory nucleus (cortex). Brain Res. Rev. 50: 305-335.
35. Haberly, L.B. & J.L. Price 1978. Association and commissural fiber systems of the olfactory cortex of the rat. II. Systems originating in the olfactory peduncle. J. Comp. Neurol. 181: 781-807.
36. Reyher, C.K., W.K. Schwerdtfeger & H.G. Baumgarten 1988. Interbulbar axonal collateralization and morphology of anterior olfactory nucleus neurons in the rat. Brain Res. Bull. 20: 549-566.
37. Keller, M. et al 2009. The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behav. Brain Res. 200: 268-276.
38. Spehr, M. et al 2006. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. J. Neurosci. 26: 1961-1970.
39. Liberles, S.D. & L.B. Buck 2006. A second class of chemosensory receptors in the olfactory epithelium. Nature 442: 645-650.
40. Dulac, C. & A.T. Torello 2003. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat. Rev. Neurosci. 4: 551-562.
41. Gelez, H. & C. Fabre-Nys 2006. Neural pathways involved in the endocrine response of anestrous ewes to the male or its odor. Neuroscience 140: 791-800.
42. Staples, L.G. et al 2005. Neural activation during cat odor-induced conditioned fear and 'trial 2' fear in rats. Neurosci. Biobehav. Rev. 29: 1265-1277.
43. Staples, L.G. et al 2008. Cat odor, but not trimethylthiazoline (fox odor), activates accessory olfactory and defense-related brain regions in rats. Neuroscience 151: 937-947.
44. Ueta, Y. et al 2005. Transgenic expression of enhanced green fluorescent protein enables direct visualization for physiological studies of vasopressin neurons and isolated nerve terminals of the rat. Endocrinology 146: 406-413.
45. De Vries, G.J. & H.A. al-Shamma 1990. Sex differences in hormonal responses of vasopressin pathways in the rat brain. J. Neurobiol. 21: 686-693.
46. Lledo, P.M., F.T. Merkle & A. Alvarez-Buylla 2008. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 31: 392-400.
47. Batista-Brito, R. et al 2008. The distinct temporal origins of olfactory bulb interneuron subtypes. J. Neurosci. 28: 3966-3975.
48. Szot, P., T.L. Bale & D.M. Dorsa 1994. Distribution of messenger RNA for the vasopressin V1a receptor in the CNS of male and female rats. Mol. Brain Res. 24: 1-10.
49. Vaccari, C., S.J. Lolait & N.L. Ostrowski 1998. Comparative distribution of vasopressin V1b and oxytocin receptor messenger ribonucleic acids in brain. Endocrinology 139: 5015-5033.
50. Ostrowski, N.L., S.J. Lolait & W.S. Young, 3rd. 1994. Cellular localization of vasopressin V1a receptor messenger ribonucleic acid in adult male rat brain, pineal, and brain vasculature. Endocrinology 135: 1511-1528.
51. Tribollet, E. et al 1988. Localization and pharmacological characterization of high affinity binding sites for vasopressin and oxytocin in the rat brain by light microscopic autoradiography. Brain Res. 442: 105-118.
52. Dluzen, D.E. et al 1998. The effects of infusion of arginine vasopressin, oxytocin, or their antagonists into the olfactory bulb upon social recognition responses in male rats. Peptides 19: 999-1005.
53. Engelmann, M., C.T. Wotjak & R. Landgraf 1995. Social discrimination procedure: an alternative method to investigate juvenile recognition abilities in rats. Physiol. Behav. 58: 315-321.
54. Engelmann, M. & R. Landgraf 1994. Microdialysis administration of vasopressin into the septum improves social recognition in Brattleboro rats. Physiol. Behav. 55: 145-149.
55. Ludwig, M. & G. Leng 1997. Autoinhibition of supraoptic nucleus vasopressin neurons in vivo: a combined retrodialysis/electrophysiological study in rats. Eur. J. Neurosci. 9: 2532-2540.
56. Bozon, B. et al 2003. MAPK, CREB and zif268 are all required for the consolidation of recognition memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358: 805-814.
57. Staples, L.G. et al 2008. Rats discriminate individual cats by their odor: possible involvement of the accessory olfactory system. Neurosci. Biobehav. Rev. 32: 1209-1217.
58. Shepherd, G.M. & C.A. Greer 1998. Olfactory bulb. In The Synaptic Organization of the Brain.G.M. Shepherd, Ed.: 159-203. Oxford University Press Inc. New York
59. Dluzen, D.E., S. Muraoka & R. Landgraf 1998. Olfactory bulb norepinephrine depletion abolishes vasopressin and oxytocin preservation of social recognition responses in rats. Neurosci. Lett. 254: 161-164.
60. Jiang, M. et al 1996. Activation of locus coeruleus enhances the responses of olfactory bulb mitral cells to weak olfactory nerve input. J. Neurosci. 16: 6319-6329.
61. Todoroki, M. et al 2010. Induction of the arginine vasopressin-enhanced green fluorescent protein fusion transgene in the rat locus coeruleus. Stress 13: 281-291.
62. Levy, F. et al 1995. Oxytocin and vasopressin release in the olfactory bulb of parturient ewes: changes with maternal experience and effects on acetylcholine, gamma-aminobutyric acid, glutamate and noradrenaline release. Brain Res. 669: 197-206.
63. Zaborszky, L. et al 1986. Cholinergic and GABAergic afferents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band. J. Comp. Neurol. 243: 488-509.
64. Ferreira, G. et al 2001. Extensive immunolesions of basal forebrain cholinergic system impair offspring recognition in sheep. Neuroscience 106: 103-116.
65. Mandairon, N. et al 2006. Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats. Eur. J Neurosci. 24: 3234-3244.
66. Ludwig, M. et al 2005. Regulation of activity-dependent dendritic vasopressin release from rat supraoptic neurons. J. Physiol. 564: 515-522.
67. Castel, M., J. Morris & M. Belenky 1996. Non-synaptic and dendritic exocytosis from dense-cored vesicles in the suprachiasmatic nucleus. Neuroreport 7: 543-547.
68. Engelmann, M., R. Landgraf & C.T. Wotjak 2004. The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary-adrenal axis under stress: an old concept revisited. Front. Neuroendocrinol. 25: 132-149.
69. Leng, G. & M. Ludwig 2008. Neurotransmitters and peptides: whispered secrets and public announcements. J. Physiol. 586: 5625-5632.
70. Ludwig, M. et al 2002. Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites. Nature 418: 85-89.
71. Uchida, N. et al 2000. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat. Neurosci. 3: 1035-1043.
72. Haberly, L.B. 2001. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26: 551-576.
73. Ludwig, M. & G. Leng 2006. Dendritic peptide release and peptide-dependent behaviours. Nat. Rev. Neurosci. 7: 126-136.
74. Engelmann, M. et al 1998. Endogenous oxytocin is involved in short-term olfactory memory in female rats. Behav. Brain Res. 90: 89-94.
75. Noack, J. et al 2010. Different importance of the volatile and non-volatile fractions of an olfactory signature for individual social recognition in rats versus mice and short-term versus long-term memory. Neurobiol. Learn. Mem. 94: 568-575.
76. Bluthe, R.M. & R. Dantzer 1990. Social recognition does not involve vasopressinergic neurotransmission in female rats. Brain Res. 535: 301-304.
77. Bluthe, R.M., J. Schoenen & R. Dantzer 1990. Androgen-dependent vasopressinergic neurons are involved in social recognition in rats. Brain Res. 519: 150-157.
78. Engelmann, M. et al 1996. Behavioral consequences of intracerebral vasopressin and oxytocin: focus on learning and memory. Neurosci. Biobehav. Rev. 20: 341-358.
79. Burman, O.H.P. & M. Mendl 2006. Long-term social memory in the laboratory rat (Rattus norvegicus). Anim. Welfare 15: 379-382.
80. Moura, P.J., S.T. Meirelles & G.F. Xavier 2010. Long-term social recognition memory in adult male rats: factor analysis of the social and non-social behaviors. Braz. J. Med. Biol. Res. 43: 663-676.
81. Popik, P. & J.M. Van Ree 1992. Long-term facilitation of social recognition in rats by vasopressin related peptides: a structure-activity study. Life Sci. 50: 567-572.
82. Yu, G.Z. et al 1996. The olfactory bulb: a critical site of action for oxytocin in the induction of maternal behaviour in the rat. Neuroscience 72: 1083-1088.
83. Dluzen, D.E. et al 2000. Oxytocin induces preservation of social recognition in male rats by activating alpha-adrenoceptors of the olfactory bulb. Eur. J. Neurosci. 12: 760-766.
84. Meddle, S.L. et al 2007. Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain. Endocrinology 148: 5095-5104.
85. Gimpl, G. & F. Fahrenholz 2001. The oxytocin receptor system: structure, function, and regulation. Physiol. Rev. 81: 629-683.
86. Goodson, J.L. & A.H. Bass 2001. Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res. Rev. 35: 246-265.
87. Goodson, J.L. 2005. The vertebrate social behavior network: evolutionary themes and variations. Horm. Behav. 48: 11-22.
88. Newman, S.W. 1999. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann. N.Y. Acad. Sci. 877: 242-257.
89. Lema, S.C. 2006. Population divergence in plasticity of the AVT system and its association with aggressive behaviors in a Death Valley pupfish. Horm. Behav. 50: 183-193.
90. Young, L.J. et al 1997. Species differences in V1a receptor gene expression in monogamous and nonmonogamous voles: behavioral consequences. Behav. Neurosci. 111: 599-605.
91. Fink, S., L. Excoffier & G. Heckel 2007. High variability and non-neutral evolution of the mammalian avpr1a gene. BMC Evol. Biol. 7: 176.
92. Coccaro, E.F. et al 1998. Cerebrospinal fluid vasopressin levels: correlates with aggression and serotonin function in personality-disordered subjects. Arch. Gen. Psychiatry. 55: 708-714.
93. Blanchard, R.J. et al 2005. AVP V1b selective antagonist SSR149415 blocks aggressive behaviors in hamsters. Pharmacol. Biochem. Behav. 80: 189-194.
94. Koolhaas, J.M. et al 1990. Medial amygdala and aggressive behavior: interaction between testosterone and vasopressin. Aggressive Behav. 16: 223-229.
95. Kim, S.J. et al 2002. Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol. Psychiatry 7: 503-507.
96. Wassink, T.H. et al 2004. Examination of AVPR1a as an autism susceptibility gene. Mol. Psychiatry 9: 968-972.
97. Yirmiya, N. et al 2006. Association between the arginine vasopressin 1a receptor (AVPR1a) gene and autism in a family-based study: mediation by socialization skills. Mol. Psychiatry 11: 488-494.
98. Lerner, A. & A. Bagic 2008. Olfactory pathogenesis of idiopathic Parkinson disease revisited. Mov. Disord. 23: 1076-1084.
99. Kawamura, M. & S. Koyama 2007. Social cognitive impairment in Parkinson's disease. J. Neurol. 254(Suppl. 4): IV/49-IV/53.
100. Suzuki, A. et al 2006. Disgust-specific impairment of facial expression recognition in Parkinson's disease. Brain 129: 707-717.
101. Clark, U.S., S. Neargarder & A. Cronin-Golomb 2008. Specific impairments in the recognition of emotional facial expressions in Parkinson's disease. Neuropsychologia 46: 2300-2309.
102. Thompson, R. et al 2004. The effects of vasopressin on human facial responses related to social communication. Psychoneuroendocrinology 29: 35-48.
103. Thompson, R.R. et al 2006. Sex-specific influences of vasopressin on human social communication. Proc. Natl. Acad. Sci. USA 103: 7889-7894.
104. Guastella, A.J. et al 2010. Intranasal arginine vasopressin enhances the encoding of happy and angry faces in humans. Biol. Psychiatry 67: 1220-1222.