Extending the socio-sexual brain: Arginine-vasopressin immunoreactive circuits in the telencephalon of mice

Brain Structure and Function

Volumn 219, Issue 3, 2014, Pages 1055-1081

  Otero Garcia, Marcos ^a   Martin Sanchez, Ana ^a   Fortes Marco, Lluis ^a   Martínez Ricós, Joana ^a   Agustin Pavón, Carmen ^b   Lanuza, Enrique ^a   Martínez García, Fernando ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

Amygdala; Bed nucleus of the stria terminalis; Islands of Calleja; Medial ventral striatum; Socio sexual behavior; Ventral pallidum

Indexed keywords

ARGIPRESSIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; SUBSTANCE P;

ADULT; AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANTERIOR COMMISSURE; ARTICLE; BRAIN FUNCTION; CELL DENSITY; CELLULAR DISTRIBUTION; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; COPING BEHAVIOR; CORPUS STRIATUM; CORTICAL AMYGDALA; DENDRITE; DORSOMEDIAL HYPOTHALAMIC NUCLEUS; FEMALE; GLOBUS PALLIDUS; HEMISPHERE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INNERVATION; MALE; MEDIAL AMYGDALA; MOUSE; NERVE FIBER; NEUROANATOMICAL TRACT TRACING; NONHUMAN; NUCLEUS ACCUMBENS; OLFACTORY BULB; OLFACTORY TRACT; PREOPTIC AREA; PRIORITY JOURNAL; SEX DIFFERENCE; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; STRIA TERMINALIS; SUBSTANTIA INNOMINATA; SUPRAOPTIC NUCLEUS; TELENCEPHALON; ANIMAL; ANIMAL BEHAVIOR; METABOLISM; NERVE CELL; PHYSIOLOGY; SEXUAL DEVELOPMENT; THALAMUS;

MUS;

AMYGDALA; ANIMALS; ARGININE VASOPRESSIN; BEHAVIOR, ANIMAL; FEMALE; MALE; MICE; NEURONS; SEX CHARACTERISTICS; TELENCEPHALON; THALAMUS;

EID: 84902364878     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0553-3     Document Type: Article

References (98)

1. Albers HE, Dean A, Karom MC, Smith D, Huhman KL (2006) Role of V1a vasopressin receptors in the control of aggression in Syrian hamsters. Brain Res 1073-1074:425-430
2. Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27:1-39
3. Ankarali S, Ankarali HC, Marangoz C (2009) Further evidence for the role of nitric oxide in maternal aggression: effects of L-NAME on maternal aggression towards female intruders in Wistar rats. Physiol Res 58:591-598
4. Arakawa H, Arakawa K, Deak T (2010) Oxytocin and vasopressin in the medial amygdala differentially modulate approach and avoidance behavior toward illness-related social odor. Neuroscience 171:1141-1151
5. Barbaresi P, Quaranta A, Amoroso S, Mensa E, Fabri M (2012) Immunocytochemical localization of calretinin-containing neurons in the rat periaqueductal gray and colocalization with enzymes producing nitric oxide: a double, double-labeling study. Synapse 66:291-307
6. Bester-Meredith JK, Young LJ, Marler CA (1999) Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm Behav 36:25-38 (Pubitemid 29382844)
7. Bielsky IF, Hu SB, Ren X, Terwilliger EF, Young LJ (2005) The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47:503-513 (Pubitemid 41149052)
8. Bolborea M, Ansel L, Weinert D, Steinlechner S, Pevet P, Klosen P (2010) The bed nucleus of the stria terminalis in the Syrian hamster (Mesocricetus auratus): absence of vasopressin expression in standard and wild-derived hamsters and galanin regulation by seasonal changes in circulating sex steroids. Neuroscience 165:819-830
9. Bosch OJ, Neumann ID (2010) Vasopressin released within the central amygdala promotes maternal aggression. Eur J Neurosci 31:883-891
10. Buijs RM (1978) Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Pathways to the limbic system, medulla oblongata and spinal cord. Cell Tissue Res 192:423-435
11. Bupesh M, Legaz I, Abellan A, Medina L (2011) Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J Comp Neurol 519:1505-1525
12. Caffe AR, van Leeuwen FW (1983) Vasopressin-immunoreactive cells in the dorsomedial hypothalamic region, medial amygdaloid nucleus and locus coeruleus of the rat. Cell Tissue Res 233:23-33 (Pubitemid 13033589)
13. Campbell P, Ophir AG, Phelps SM (2009) Central vasopressin and oxytocin receptor distributions in two species of singing mice. J Comp Neurol 516:321-333
14. Canteras NS (2002) The medial hypothalamic defensive system: hodological organization and functional implications. Pharmacol Biochem Behav 71:481-491
15. Castel M, Morris JF (1988) The neurophysin-containing innervation of the forebrain of the mouse. Neuroscience 24:937-966
16. Caughey SD, Klampfl SM, Bishop VR, Pfoertsch J, Neumann ID, Bosch OJ, Meddle SL (2011) Changes in the intensity of maternal aggression and central oxytocin and vasopressin V1a receptors across the peripartum period in the rat. J Neuroendocrinol 23:1113-1124
17. Chamero P, Marton TF, Logan DW, Flanagan K, Cruz JR, Saghatelian A, Cravatt BF, Stowers L (2007) Identification of protein pheromones that promote aggressive behaviour. Nature 450:899-902 (Pubitemid 350231315)
18. Chamero P, Katsoulidou V, Hendrix P, Bufe B, Roberts R, Matsunami H, Abramowitz J, Birnbaumer L, Zufall F, Leinders-Zufall T (2011) G protein G(alpha)o is essential for vomeronasal function and aggressive behavior in mice. Proc Natl Acad Sci USA 108:12898-12903
19. de Vries GJ (2008) Sex differences in vasopressin and oxytocin innervation of the brain. Prog Brain Res 170:17-27
20. De Vries GJ, Buijs RM (1983) The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum. Brain Res 273:307-317 (Pubitemid 13039718)
21. De Vries GJ, Wang Z, Bullock NA, Numan S (1994) Sex differences in the effects of testosterone and its metabolites on vasopressin messenger RNA levels in the bed nucleus of the stria terminalis of rats. J Neurosci 14:1789-1794 (Pubitemid 24080026)
22. Demas GE, Eliasson MJ, Dawson TM, Dawson VL, Kriegsfeld LJ, Nelson RJ, Snyder SH (1997) Inhibition of neuronal nitric oxide synthase increases aggressive behavior in mice. Mol Med 3:610-616 (Pubitemid 27465232)
23. DeVries GJ, Buijs RM, Van Leeuwen FW, Caffe AR, Swaab DF (1985) The vasopressinergic innervation of the brain in normal and castrated rats. J Comp Neurol 233:236-254 (Pubitemid 15111241)
24. Dong HW, Swanson LW (2004) Projections from bed nuclei of the stria terminalis, posterior division: implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J Comp Neurol 471:396-433
25. Dubois-Dauphin M, Barberis C, de Bilbao F (1996) Vasopressin receptors in the mouse (Mus musculus) brain: sex-related expression in the medial preoptic area and hypothalamus. Brain Res 743:32-39 (Pubitemid 27028753)
26. Everts HG, De Ruiter AJ, Koolhaas JM (1997) Differential lateral septal vasopressin in wild-type rats: correlation with aggression. Horm Behav 31:136-144 (Pubitemid 27239868)
27. Ferris CF, Delville Y, Miller MA, Dorsa DM, De Vries GJ (1995) Distribution of small vasopressinergic neurons in golden hamsters. J Comp Neurol 360:589-598
28. Gabor CS, Phan A, Clipperton-Allen AE, Kavaliers M, Choleris E (2012) Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition. Behav Neurosci 126:97-109
29. Gammie SC (2005) Current models and future directions for understanding the neural circuitries of maternal behaviors in rodents. Behav Cogn Neurosci Rev 4:119-135
30. Garcia-Moreno F, Pedraza M, Di Giovannantonio LG, Di Salvio M, Lopez-Mascaraque L, Simeone A, De Carlos JA (2010) A neuronal migratory pathway crossing from diencephalon to telencephalon populates amygdala nuclei. Nat Neurosci 13:680-689
31. Gillard ER, Coburn CG, de Leon A, Snissarenko EP, Bauce LG, Pittman QJ, Hou B, Curras-Collazo MC (2007) Vasopressin autoreceptors and nitric oxide-dependent glutamate release are required for somatodendritic vasopressin release from rat magnocellular neuroendocrine cells responding to osmotic stimuli. Endocrinology 148:479-489 (Pubitemid 46143152)
32. Guirado S, Real MA, Davila JC (2008) Distinct immunohistochemically defined areas in the medial amygdala in the developing and adult mouse. Brain Res Bull 75:214-217 (Pubitemid 351335172)
33. Gutierrez-Castellanos N, Martinez-Marcos A, Martinez-Garcia F, Lanuza E (2010) Chemosensory function of the amygdala. Vitam Horm 83:165-196
34. Hatton GI, Yang QZ (1989) Supraoptic nucleus afferents from the main olfactory bulb - II. Intracellularly recorded responses to lateral olfactory tract stimulation in rat brain slices. Neuroscience 31:289-297 (Pubitemid 19238637)
35. Hatton GI, Yang QZ (1990) Activation of excitatory amino acid inputs to supraoptic neurons. I. Induced increases in dyecoupling in lactating, but not virgin or male rats. Brain Res 513:264-269 (Pubitemid 20132263)
36. Herkenham M (1987) Mismatches between neurotransmitter and receptor localizations in brain: observations and implications. Neuroscience 23:1-38
37. Hernando F, Schoots O, Lolait SJ, Burbach JP (2001) Immunohistochemical localization of the vasopressin V1b receptor in the rat brain and pituitary gland: anatomical support for its involvement in the central effects of vasopressin. Endocrinology 142:1659-1668 (Pubitemid 32299697)
38. Ho JM, Murray JH, Demas GE, Goodson JL (2010) Vasopressin cell groups exhibit strongly divergent responses to copulation and male-male interactions in mice. Horm Behav 58:368-377
39. Johnson AE, Barberis C, Albers HE (1995) Castration reduces vasopressin receptor binding in the hamster hypothalamus. Brain Res 674:153-158
40. Karlson P, Luscher M (1959) Pheromones: a new term for a class of biologically active substances. Nature 183:55-56
41. Kavaliers M, Choleris E, Pfaff DW (2005) Recognition and avoidance of the odors of parasitized conspecifics and predators: differential genomic correlates. Neurosci Biobehav Rev 29:1347-1359 (Pubitemid 41447517)
42. Knobloch HS, Charlet A, Hoffmann LC, Eliava M, Khrulev S, Cetin AH, Osten P, Schwarz MK, Seeburg PH, Stoop R, Grinevich V (2012) Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73:553-566
43. Koolhaas JM, Van Den Brink THC, Roozendaal B, Boorsma F (1990) Medial amygdala and aggressive behavior: interaction between testosterone and vasopressin. Aggress Behav 16:223-229 (Pubitemid 20285093)
44. Leypold BG, Yu CR, Leinders-Zufall T, Kim MM, Zufall F, Axel R (2002) Altered sexual and social behaviors in trp2 mutant mice. Proc Natl Acad Sci USA 99:6376-6381 (Pubitemid 34493319)
45. Lim MM, Young LJ (2004) Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience 125:35-45 (Pubitemid 38402157)
46. Lim MM, Murphy AZ, Young LJ (2004) Ventral striatopallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (Microtus ochrogaster) . J Comp Neurol 468:555-570 (Pubitemid 38036695)
47. Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ (2011) Functional identification of an aggression locus in the mouse hypothalamus. Nature 470:221-226
48. Ludwig M, Leng G (2006) Dendritic peptide release and peptide-dependent behaviours. Nat Rev Neurosci 7:126-136 (Pubitemid 43151599)
49. Manning M, Misicka A, Olma A, Bankowski K, Stoev S, Chini B, Durroux T, Mouillac B, Corbani M, Guillon G (2012) Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. J Neuroendocrinol 24:609-628
50. Martínez-García F, Novejarque A, Gutiérrez- Castellanos N, Lanuza E (2012) Chapter 6 - Piriform cortex and amygdala. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Academic Press, San Diego, pp 140-172
51. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE (2003) Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144:2055-2067 (Pubitemid 36543346)
52. Modney BK, Yang QZ, Hatton GI (1990) Activation of excitatory amino acid inputs to supraoptic neurons. II. Increased dyecoupling in maternally behaving virgin rats. Brain Res 513:270-273 (Pubitemid 20132264)
53. Moncho-Bogani J, Lanuza E, Hernandez A, Novejarque A, Martinez-Garcia F (2002) Attractive properties of sexual pheromones in mice. Innate or learned? Physiol Behav 77:167-176 (Pubitemid 35245734)
54. Murakami G, Hunter RG, Fontaine C, Ribeiro A, Pfaff D (2011) Relationships among estrogen receptor, oxytocin and vasopressin gene expression and social interaction in male mice. Eur J Neurosci 34:469-477
55. Murray EK, Varnum MM, Fernandez JL, de Vries GJ, Forger NG (2011) Effects of neonatal treatment with valproic acid on vasopressin immunoreactivity and olfactory behaviour in mice. J Neuroendocrinol 23:906-914
56. Napier TC, Mitrovic I, Churchill L, Klitenick MA, Lu XY, Kalivas PW (1995) Substance P in the ventral pallidum: projection from the ventral striatum, and electrophysiological and behavioral consequences of pallidal substance P. Neuroscience 69:59-70
57. Nephew BC, Bridges RS (2008) Arginine vasopressin V1a receptor antagonist impairs maternal memory in rats. Physiol Behav 95:182-186
58. Newman SW (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
59. Novejarque A, Gutierrez-Castellanos N, Lanuza E, Martinez-Garcia F (2011) Amygdaloid projections to the ventral striatum in mice: direct and indirect chemosensory inputs to the brain reward system. Front Neuroanat. doi:10.3389/fnana.2011.00054
60. Olucha-Bordonau FE, Teruel V, Barcia-Gonzalez J, Ruiz-Torner A, Valverde-Navarro AA, Martinez-Soriano F (2003) Cytoarchitecture and efferent projections of the nucleus incertus of the rat. J Comp Neurol 464:62-97 (Pubitemid 36899037)
61. Pardo-Bellver C, Cadiz-Moretti B, Novejarque A, Martinez-Garcia F, Lanuza E (2012) Differential efferent projections of the anterior, posteroventral, and posterodorsal subdivisions of the medial amygdala in mice. Front Neuroanat. doi:10.3389/fnana.2012.00033
62. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic Press, San Diego
63. Pecina S, Berridge KC (2000) Opioid site in nucleus accumbens shell mediates eating and hedonic 'liking' for food: map based on microinjection Fos plumes. Brain Res 863:71-86 (Pubitemid 30201586)
64. Pecina S, Berridge KC (2005) Hedonic hot spot in nucleus accumbens shell: where do mu-opioids cause increased hedonic impact of sweetness? J Neurosci 25:11777-11786 (Pubitemid 43098470)
65. Plumari L, Viglietti-Panzica C, Allieri F, Honda S, Harada N, Absil P, Balthazart J, Panzica GC (2002) Changes in the arginine-vasopressin immunoreactive systems in male mice lacking a functional aromatase gene. J Neuroendocrinol 14:971-978 (Pubitemid 36024595)
66. Popeski N, Woodside B (2004) Central nitric oxide synthase inhibition disrupts maternal behavior in the rat. Behav Neurosci 118:1305-1316 (Pubitemid 39578477)
67. Riedel A, Hartig W, Seeger G, Gartner U, Brauer K, Arendt T (2002) Principles of rat subcortical forebrain organization: a study using histological techniques and multiple fluorescence labeling. J Chem Neuroanat 23:75-104 (Pubitemid 34159078)
68. Risold PY, Swanson LW (1997) Connections of the rat lateral septal complex. Brain Res Brain Res Rev 24:115-195 (Pubitemid 27461311)
69. Roberts SA, Simpson DM, Armstrong SD, Davidson AJ, Robertson DH, McLean L, Beynon RJ, Hurst JL (2010) Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biol 8:75
70. Rood BD, de Vries GJ (2011) Vasopressin innervation of the mouse (Mus musculus) brain and spinal cord. J Comp Neurol 519:2434-2474
71. Rood BD, Murray EK, Laroche J, Yang MK, Blaustein JD, De Vries GJ (2008) Absence of progestin receptors alters distribution of vasopressin fibers but not sexual differentiation of vasopressin system in mice. Neuroscience 154:911-921
72. Rood BD, Stott RT, You S, Smith CJ, Woodbury ME, de Vries GJ (2012-2013) Site of origin of and sex differences in the vasopressin innervation of the mouse (Mus musculus) brain. J Comp Neurol
73. Rosen GJ, De Vries GJ, Villalba C, Weldele ML, Place NJ, Coscia EM, Glickman SE, Forger NG (2006) Distribution of vasopressin in the forebrain of spotted hyenas. J Comp Neurol 498:80-92 (Pubitemid 44198735)
74. Rosen GJ, De Vries GJ, Goldman SL, Goldman BD, Forger NG (2007) Distribution of vasopressin in the brain of the eusocial naked mole-rat. J Comp Neurol 500:1093-1105 (Pubitemid 46106467)
75. Schorscher-Petcu A, Dupre A, Tribollet E (2009) Distribution of vasopressin and oxytocin binding sites in the brain and upper spinal cord of the common marmoset. Neurosci Lett 461:217-222
76. Shipley MT, Adamek GD (1984) The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res Bull 12:669-688 (Pubitemid 14065432)
77. Smithson KG, Weiss ML, Hatton GI (1989) Supraoptic nucleus afferents from the main olfactory bulb - I. Anatomical evidence from anterograde and retrograde tracers in rat. Neuroscience 31:277-287 (Pubitemid 19238636)
78. Smithson KG, Weiss ML, Hatton GI (1992) Supraoptic nucleus afferents from the accessory olfactory bulb: evidence from anterograde and retrograde tract tracing in the rat. Brain Res Bull 29:209-220
79. Stoop R (2012) Neuromodulation by oxytocin and vasopressin. Neuron 76:142-159
80. Szot P, Dorsa DM (1993) Expression of vasopressin mRNA in extrahypothalamic nuclei of the homozygous Brattleboro rat is not modulated by testosterone. Neuroendocrinology 58:381-387 (Pubitemid 23330184)
81. Toth M, Fuzesi T, Halasz J, Tulogdi A, Haller J (2010) Neural inputs of the hypothalamic "aggression area" in the rat. Behav Brain Res 215:7-20
82. Tsukahara S, Tsuda MC, Kurihara R, Kato Y, Kuroda Y, Nakata M, Xiao K, Nagata K, Toda K, Ogawa S (2011) Effects of aromatase or estrogen receptor gene deletion on masculinization of the principal nucleus of the bed nucleus of the stria terminalis of mice. Neuroendocrinology 94:137-147
83. Ubeda-Banon I, Novejarque A, Mohedano-Moriano A, Pro-Sistiaga P, de la Rosa-Prieto C, Insausti R, Martinez-Garcia F, Lanuza E, Martinez-Marcos A (2007) Projections from the posterolateral olfactory amygdala to the ventral striatum: neural basis for reinforcing properties of chemical stimuli. BMC Neurosci 8:103
84. Ubeda-Banon I, Novejarque A, Mohedano-Moriano A, Pro-Sistiaga P, Insausti R, Martinez-Garcia F, Lanuza E, Martinez-Marcos A (2008) Vomeronasal inputs to the rodent ventral striatum. Brain Res Bull 75:467-473 (Pubitemid 351343840)
85. Veenema AH, Neumann ID (2007) Neurobiological mechanisms of aggression and stress coping: a comparative study in mouse and rat selection lines. Brain Behav Evol 70:274-285 (Pubitemid 47525208)
86. Veinante P, Freund-Mercier MJ (1997) Distribution of oxytocin- and vasopressin-binding sites in the rat extended amygdala: a histoautoradiographic study. J Comp Neurol 383:305-325 (Pubitemid 27280078)
87. Wang Z (1995) Species differences in the vasopressin-immunoreactive pathways in the bed nucleus of the stria terminalis and medial amygdaloid nucleus in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus) . Behav Neurosci 109:305-311
88. Wang Z, Smith W, Major DE, De Vries GJ (1994) Sex and species differences in the effects of cohabitation on vasopressin messenger RNA expression in the bed nucleus of the stria terminalis in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Brain Res 650:212-218 (Pubitemid 24207065)
89. Wang Z, Zhou L, Hulihan TJ, Insel TR (1996) Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: a quantitative comparative study. J Comp Neurol 366:726-737 (Pubitemid 26087304)
90. Wang Z, Moody K, Newman JD, Insel TR (1997a) Vasopressin and oxytocin immunoreactive neurons and fibers in the forebrain of male and female common marmosets (Callithrix jacchus). Synapse 27:14-25 (Pubitemid 27327598)
91. Wang Z, Toloczko D, Young LJ, Moody K, Newman JD, Insel TR (1997b) Vasopressin in the forebrain of common marmosets (Callithrix jacchus): studies with in situ hybridization, immunocytochemistry and receptor autoradiography. Brain Res 768:147-156 (Pubitemid 27433487)
92. Wersinger SR, Kelliher KR, Zufall F, Lolait SJ, O'Carroll AM, Young WS 3rd (2004) Social motivation is reduced in vasopressin 1b receptor null mice despite normal performance in an olfactory discrimination task. Horm Behav 46:638-645 (Pubitemid 39535145)
93. Wersinger SR, Caldwell HK, Christiansen M, Young WS 3rd (2007a) Disruption of the vasopressin 1b receptor gene impairs the attack component of aggressive behavior in mice. Genes Brain Behav 6:653-660 (Pubitemid 47476187)
94. Wersinger SR, Caldwell HK, Martinez L, Gold P, Hu SB, Young WS 3rd (2007b) Vasopressin 1a receptor knockout mice have a subtle olfactory deficit but normal aggression. Genes Brain Behav 6:540-551 (Pubitemid 47246220)
95. Yang QZ, Hatton GI (1988) Direct evidence for electrical coupling among rat supraoptic nucleus neurons. Brain Res 463:47-56
96. Young LJ, Winslow JT, Nilsen R, Insel TR (1997) Species differences in V1a receptor gene expression in monogamous and nonmonogamous voles: behavioral consequences. Behav Neurosci 111:599-605 (Pubitemid 27251329)
97. Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR (1999a) Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400:766-768 (Pubitemid 29399537)
98. Young LJ, Toloczko D, Insel TR (1999b) Localization of vasopressin (V1a) receptor binding and mRNA in the rhesus monkey brain. J Neuroendocrinol 11:291-297 (Pubitemid 29149883)