Anatomical and neurochemical definition of the nucleus of the stria terminalis in Japanese quail (Coturnix japonica)

Journal of Comparative Neurology

Volumn 396, Issue 2, 1998, Pages 141-157

  Aste, N ^a,d   Balthazart, J ^b   Absil, P ^b   Grossmann, R ^c   Mulhbauer E ^c   Viglietti Panzica, C ^a   Panzica, G C ^a,e  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^d SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^e Dept Anat Pharmacol/Forensic M   (Italy)

Author keywords

Aromatase; Bird; In situ hybridization; Sex dimorphism; Vasotocin

Indexed keywords

ARGIPRESTOCIN; AROMATASE;

ANIMAL TISSUE; ARTICLE; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; QUAIL; SEX DIFFERENCE; STRIA TERMINALIS;

ANIMALS; AROMATASE; BRAIN MAPPING; COTURNIX; FEMALE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MAMMALS; SEX CHARACTERISTICS; SPECIES SPECIFICITY; STAINING AND LABELING; VASOTOCIN;

EID: 0032578011     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980629)396:2<141::AID-CNE1>3.0.CO;2-0     Document Type: Article

References (123)

1. Akesson, T.R., R.B. Simerly, and P.E. Micevych (1988) Estrogen-concentrating hypothalamic and limbic neurons project to the medial preoptic nucleus. Brain Res. 451:381-385.
2. Allen, L.S. and R.A. Gorski (1990) Sex difference in the bed nucleus of the stria terminalis of the human brain. J. Comp. Neurol. 302:697-706.
3. Anderson, K.D. and A. Reiner (1991) Striatonigral projection neurons: A retrograde labeling study of the percentages that contain substance P or enkephalin in pigeons. J. Comp. Neurol. 303:658-673.
4. Arends, J.J.A., J.M. Wild, and H.P. Zeigler (1988) Projections of the nucleus of the tractus solitarius in the pigeon. J. Comp. Neurol. 278:405-429.
5. Aste, N., C. Viglietti-Panzica, A. Fasolo, and G.C. Panzica (1995) Mapping of neurochemical markers in quail central nervous system: VIP- and SP-like immunoreactivity. J. Chem. Neuroanat. 8:87-102.
6. Aste, N., E. Mühlbauer, and R. Grossmann (1996) Distribution of AVT gene expressing neurons in the prosencephalon of japanese quail and chicken. Cell Tissue Res. 286:365-373.
7. Aste, N., C. Viglietti-Panzica, J. Balthazart, and G.C. Panzica (1997) Testosterone modulation of peptidergic pathways in the septo-preoptic region of male Japanese quail. Poultry Avian Biol. Rev. 8:9-20.
8. Azumaya, Y. and K. Tsutsui (1996) Localization of galanin and its binding sites in the quail brain. Brain Res. 727:187-195.
9. Balthazart, J. (1997) Steroid control and sexual differentiation of brain aromatase. J. Steroid Biochem. Mol. Biol. 61:323-339.
10. Balthazart, J. and P. Absil (1997) Identification of catecholaminergic inputs to and outputs from aromatase-containing brain areas of the Japanese quail by tract tracing combined with tyrosine hydroxylase immunocytochemistry. J. Comp. Neurol. 382:401-428.
11. Balthazart, J. and G.F. Ball (1997) Neuroendocrine regulation of appetitive and consummatory aspects of male sexual behavior in Japanese quail. In S. Harvey, R. Etches (eds): Perspectives in Avian Endocrinology. Bristol, United Kingdom: Journal of Endocrinology Ltd., pp. 241-255.
12. Balthazart, J. and A. Foidart (1993) Neural bases of behavioral sex differences in quail. In M. Haug (ed): The development of sex differences and similarities in behavior. Amsterdam: Kluwer Academic Pubishers, pp. 51-75.
13. Balthazart, J. and E. Schofieniels (1979) Pheromones are involved in the control of sexual behaviour in birds. Naturwissenschaften 66:55-56.
14. Balthazart, J. and C. Surlemont (1990a) Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail preoptic area. Brain Res. Bull. 25:7-14.
15. Balthazart, J. and C. Surlemont (1990b) Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol. Behav. 48:599-609.
16. Balthazart, J., M. Gahr, and C. Surlemont (1989) Distribution of estrogen receptors in the brain of the Japanese quail: An immunocytochemical study. Brain Res. 501:205-214.
17. Balthazart, J., A. Foidart, and N. Harada (1990a) Immunocytochemical localization of aromatase in the brain. Brain Res. 514:327-333.
18. Balthazart, J., A. Foidart, C. Surlemont, A. Vockel, and N. Harada (1990b) Distribution of aromatase in the brain of the Japanese quail, ring dove, and zebra finch: An immunocytochemical study. J. Comp. Neurol. 301:276-288.
19. Balthazart, J., A. Foidart, C. Surlemont, N. Harada, and F. Naftolin (1992a) Neuroanatomical specificity in the autoregulation of aromatase-immunoreactive neurons by androgens and estrogens. An immunocytochemical study. Brain Res. 574:280-290.
20. Balthazart, J., A. Foidart, E.M. Wilson, and G.F. Ball (1992b) Immunocytochemical localization of androgen receptors in the male songbird and quail brain. J. Comp. Neurol. 317:407-420.
21. Balthazart, J., V. Dupiereux, N. Aste, C. Viglietti-Panzica, M. Barrese, and G.C. Panzica (1994) Afferent and efferent connections of the sexually dimorphic medial preoptic nucleus of the male quail revealed by in vitro transport of DiI. Cell Tissue Res. 276:455-475.
22. Balthazart, J., P. Absil, A. Foidart, M. Houbart, N. Harada, and G.F. Ball (1996a) Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): Implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J. Neurobiol. 31:129-148.
23. Balthazart, J., A. Foidart, P. Absil, and N. Harada (1996b) Effects of testosterone and its metabolites on aromatase-immunoreactive cells in the quail brain: Relationship with the activation of male reproductive behavior. J. Steroid Biochem. Mol. Biol. 56:185-200.
24. Balthazart, J., P. Absil, C. Viglietti-Panzica, and G.C. Panzica (1997) Vasotocinergic innervation of areas containing aromatase-immunoreactive cells in the quail forebrain. J. Neurobiol. 33:45-60.
25. Baylé, J.D., F. Ramade, and J. Oliver (1974) Stereotaxic topography of the brain of the quail (Coturnix coturnix japonica). J. Physiol. (Paris) 68:219-241.
26. Berk, M.L. (1987) Projections of the lateral hypothalamus and bed nucleus of the stria terminalis to the dorsal vagal complex in the pigeon. J. Comp. Neurol. 260:140-156.
27. Brauth, S.E., J.L. Ferguson, and C.A. Kitt (1978) Prosencephalic pathways related to the paleostriatum of the pigeon (Columba livia). Brain Res. 147:205-221.
28. Breazile, J.E. and W.J. Kuenzel (1993) Systema nervosum centrale. In J.J. Baumel, A.S. King, J.E. Breazile, H.E. Evans, and J.C. Vanden Berge (eds): Handbook of Avian Anatomy: Nomina Anatomicum Avium. Cambridge, MA: Nuttall Ornithological Club, pp. 493-554.
29. Brot, M.D., G.J. De Vries, and D.M. Dorsa (1993) Local implants of testosterone metabolites regulate vasopressin mRNA in sexually dimorphic nuclei of the rat brain. Peptides 14:933-940.
30. Burne, T.H.J. and L.J. Rogers (1996) Responses to odorants by the domestic chick. Physiol. Behav. 60:1441-1447.
31. Ganteras, N.S., R.B. Simerly, and L.W. Swanson (1995) Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat. J. Comp. Neurol. 360:213-245.
32. Castagna, C., P. Absil, A. Foidart, and J. Balthazart (1998) Systemic and intracerebroventricular injections of vasotocin inhibit appetitive and consummatory components of male sexual behavior in Japanese quail. Behav. Neurosci. (in press)
33. Claro, F., S. Segovia, A. Guilamón, and A. Del Abril (1995) Lesions in the medial posterior region of the BST impair sexual behavior in sexually experienced and inexperienced male rats. Brain Res. Bull. 36:1-10.
34. De Olmos, J. and W.R. Ingram (1972) The projection fields of the stria terminalis in the rat brain. An experimental study. J. Comp. Neurol. 146:303-334.
35. De Olmos, J., H. Hardy, and L. Heimer (1978) The afferent connections of the main and accessory olfactory bulb formation in the rat: An experimental and HRP-study. J. Comp. Neurol. 181:213-244.
36. De Olmos, J., G.F. Alheid, and C.A. Beltramino (1985) Amygdala. In G. Paxinos (ed): The Rat Nervous System, Vol 1. Forebrain and Midbrain. Orlando, FL: Academic Press, pp. 223-334.
37. De Vries, G.J. (1995) Studying neurotransmitter systems to understand the development and function of sex differences in the brain: The case of vasopressin. In P. Micevich and R.P. Hammer (eds): Neurobiological effects of sex steroid hormones. Cambridge, Ma: Cambridge University Press, pp. 254-278.
38. De Vries, G.J. and H.A. Al Shamma (1990) Sex differences in hormonal responses of vasopressin pathways in the rat brain. J. Neurobiol. 21:686-693.
39. De Vries, G.J. and R.M. Buijs (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.
40. De Vries, G.J. and W. Duetz (1984) Sex steroid effects on the vasopressin innervation of the adult rat brain. Neurosci. Lett, 18(Suppl.):343.
41. De Vries, G.J., R.M. Buijs, and F.W. Van Leeuwen (1984) Sex differences in vasopressin and other neurotransmitter systems in the brain. Progr. Brain Res. 61:185-203.
42. De Vries, G.J., R.M. Buijs, F.W. Van Leeuwen, A.R. Gaffé, and D.F. Swaab (1985) The vasopressinergic innervation of the brain in normal and castrated rats. J. Comp. Neurol. 233:236-254.
43. De Vries, G.J., W. Duetz, R.M. Buijs, J. Van Heerikhuize, and J.Y.M. Vreeburg (1986) Effects of androgens and estrogens on the vasopressin and oxytocin innervation of the adult rat brain. Brain Res. 399:296-302.
44. De Vries, G.J., H.A. Al Shamma, and L. Zhou (1994a) The sexually dimorphic vasopressin innervation of the brain as a model for steroid modulation of neuropeptide transmission. In V.N. Luine and C.F. Harding (eds): Hormonal Restructuring of the Adult Brain. Basic and Clinical Perspectives. Ann. NYAcad. Sci., Vol. 743. New York: New York Academy of Sciences, pp. 95-120.
45. De Vries, G.J., Z. Wang, N.A. Bullock, and S. Numan (1994b) 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.
46. Del Abril, A., S. Segovia, and A. Guillamon (1987) The bed nucleus of the stria terminalis in the rat: Regional sex differences controlled by gonadal steroids early after birth. Dev. Brain Res. 32:295-300.
47. Deviche, P., E. García-Ojeda, L. Plumari, and G.C. Panzica (1996) Vasotocinergic innervation in a male passerine bird (Junco hyemalis): Effect of photoperiodic condition. Soc. Neurosci. Abstr. 22:1551.
48. Emery, D.E. and B.D. Sachs (1976) Copulatory behavior in male rats with lesions in the bed nucleus of the stria terminalis. Physiol. Behav. 17:803-806.
49. Ferris, C.F., Y. Delville, M.A. Miller, D.M. Dorsa, and G.J. De Vries (1995) Distribution of small vasopressinergic neurons in golden hamsters. J. Comp. Neurol. 360:589-598.
50. Foidart, A., A. De Clerck, N. Harada, and J. Balthazart (1994) Aromatase-immunoreactive cells in the quail brain: Effects of testosterone and sex dimorphism. Physiol. Behav. 55:453-464.
51. Foidart, A., N. Harada, and J. Balthazart (1995a) Aromatase-immunoreactive cells are present in mouse brain areas that are known to express high levels of aromatase activity. Cell Tissue Res. 280:561-574.
52. Foidart, A., J. Reid, P. Absil, N. Yoshimura, N. Harada, and J. Balthazart (1995b) Critical reexamination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. J. Chem. Neuroanat. 8:267-282.
53. Gahr, M. (1997) How should brain nuclei be delineated? Consequences for developmental mechanisms and for correlations of area size, neuron numbers and functions of brain nuclei. Trends Neurosci. 20:58-62.
54. Gray, D.A. and E. Simon (1983) Mammalian and avian antidiuretic hormone: Studies related to possible species variation in osmoregulatory systems. J. Comp. Physiol. A 151:241-246.
55. Guillamon, A. and S. Segovia (1997) Sex differences in the vomeronasal system. In G.C. Panzica and J. Balthazart (eds): Hormones, Brain, and Behavior. Brain Res. Bull. 44:377-382.
56. Hadeishi, Y. and R.I. Wood (1996) Nitric oxide synthase in mating behavior circuitry of male Syrian hamster brain. J. Neurobiol. 30:480-492.
57. Hamann, D., N. Hunt, and R. Ivell (1992) The chicken vasotocin gene. J. Neuroendocrinol. 4:505-513.
58. Hines, M., L.S. Allen, and R.A. Gorski (1992) Sex differences in subrogions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis of the rat. Brain Res. 579:321-326.
59. Jakab, R.L., T.L. Horvath, C. Leranth, N. Harada, and F. Naftolin (1993) Aromatase immunoreactivity in the rat brain: Gonadectomy-sensitive hypothalamic neurons and an unresponsive "limbic ring" of the lateral septum-bed nucleus-amygdala complex. J. Steroid Biochem. Mol. Biol. 44:481-498.
60. Jones, R.B. and T.J. Roper (1997) Olfaction in the domestic fowl: A critical review. Physiol. Behav. 62:1009-1018.
61. Jurkevich, A., S.W. Barth, N. Aste, G.C. Panzica, and R. Grossmann (1996) Intracerebral sex differences in the vasotocin system in birds: Possible implication on behavioral and autonomie functions. Hormone Behav. 30:673-681.
62. Jurkevich, A., S.W. Barth, and R. Grossmann (1997) Sexual dimorphism of arg-vasotocin gene expressing neurons in the telencephalon and dorsal diencephalon of the domestic fowl. An immunocytochemical and in situ hybridization study. Cell Tissue Res. 287:69-77.
63. Karten, H.J. and W. Hodos (1967) A Stereotaxis Atlas of the Brain of the Pigeon (Columba livia). Baltimore: The John Hopkins University Press.
64. Kiss, J.Z., T.A.M. Voorhuis, J.A.M. Van Eekelen, E.R. De Kloet, and D. De Wied (1987) Organization of vasotocin-immunoreactive cells and fibers in the canary brain. J. Comp. Neurol. 263:347-364.
65. Kitt, C.A. and S.E. Brauth (1986a) Telencephalic projections from midbrain and isthmal cell groups in the pigeon. I. Locus coeruleus and subcoeruleus. J. Comp. Neurol. 247:69-91.
66. Kitt, C.A. and S.E. Brauth (1986b) Telencephalic projections from midbrain and isthmal cell groups in the pigeon. II. The nigral complex. J. Comp. Neurol. 247:92-110.
67. Krettek, J.E. and J.L. Price (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J. Comp. Neurol. 178:225-254.
68. Kuenzel, W.J. and M. Masson (1988) A Stereotaxic Atlas of the Brain of the Chick (Gallus domesticus). Baltimore, London: The Johns Hopkins University Press.
69. Lauber, M.E. and W. Lichtensteiger (1994) pre and postnatal ontogeny of aromatase cytochrome P450 messenger ribonucleic acid expression in the male rat brain studied by in situ hybridization. Endocrinology 135:1661-1668.
70. Lopez, H.S. and H.F. Carrer (1982) Investigations of peripeduncular-hypothalamic pathways involved in the control of lordosis in rat. Brain Res. 253:287-302.
71. Medina, L. and A. Reiner (1997) The efferent projections of the dorsal and ventral pallidal parts of the pigeon basal ganglia, studied with biotinylated dextran amine. Neuroscience 81:773-802.
72. Miller, M.A., L. Vician, D.K. Clifton, and D.M. Dorsa (1989) Sex differences in vasopressin neurons in the bed nucleus of the stria terminalis by in situ hybridization. Peptides 10:615-619.
73. Moga, M.M., C.B. Saper, and T.S. Gray (1989) Bed nucleus of the stria terminalis: Cytoarchitecture, immunohistochemistry, and projection to the parabrachial nucleus in the rat. J. Comp. Neurol. 283:315-332.
74. Numan, M. and M.J. Numan (1996) A lesion and neuroanatomical tracttracing analysis of the role of the bed nucleus of the stria terminalis in retrieval behavior and other aspects of maternal responsiveness in rats. Dev. Psychobiol. 29:23-51.
75. Panzica, G.C., C. Viglietti-Panzica, A. Fasolo, and F. Vandesande (1986) CRF-like immunoreactive system in the quail brain. J.Hirnforsch. 27:539-547.
76. Panzica, G.C., C. Viglietti-Panzica, F. Sánchez, P. Sante, and J. Balthazart (1991) Effects of testosterone on a selected neuronal population within the preoptic sexually dimorphic nucleus of the Japanese quail. J. Comp. Neurol. 303:443-456.
77. Panzica, G.C., N. Aste, C. Viglietti-Panzica, and A. Fasolo (1992a) Neuronal circuits controlling quail sexual behavior. Chemical neuroanatomy of the septo-preoptic region. Poultry Sci. Rev. 4:249-259.
78. Panzica, C.G., M. Barrese, N. Aste, and C. Viglietti-Panzica (1992b) Direct connections between septum and medial preoptic nucleus of the Japanese quail. A DiI study on fixed tissue [abstract]. Neurosci. Lett. 43(Suppl.):82.
79. Panzica, G.C., R. Arévalo, F. Sánchez, J.R. Alonso, N. Aste, C. Viglietti-Panzica, J. Aijón, and R. Vázquez (1994) Topographical distribution of reduced nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase in the brain of the Japanese quail. J. Comp. Neurol. 342:97-114.
80. Panzica, G.C., E. García-Ojeda, C. Viglietti Panzica, N.E. Thompson, and M.A. Ottinger (1996a) Testosterone effects on vasotocinergic innervation of sexually dimorphic medial preoptic nucleus and lateral septum during aging in male quail. Brain Res. 712:190-198.
81. Panzica, G.C., C. Viglietti-Panzica, and J. Balthazart (1996b) The sexually dimorphic medial preoptic nucleus of quail: A key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol. 17:1-75.
82. Panzica, G.C., N. Aste, C. Castagna, J. Balthazart, and C. Viglietti-Panzica (1997) Sexual dimorphism, steroid-induced plasticity, and behavioral significance of the vasotocinergic innervation of the avian brain. In H.-W. Korf and K.H. Usadel (eds): Neuroendocrinology: Retrospect and Perspectives. Berlin: Springer Verlag, pp. 127-150.
83. Papi, F. (1989) Pigeons use olfactory cues to navigate. Ethol. Ecol. Evol. 1:219-231.
84. Papi, F. (1990) Olfactory navigation in birds. Experientia 46:352-363.
85. Planas, B., P.E. Kolb, M.A. Raskind, and M.A. Miller (1994) Galanin in the bed nucleus of the stria terminalis and medial amygdala of the rat: Lack of sexual dimorphism despite regulation of gene expression across puberty. Endocrinology 134:1999-2004.
86. Planas, B., P.E. Kolb, M.A. Raskind, and M.A. Miller (1995) Sex difference in coexpression by galanin neurons accounts for sexual dimorphism of vasopressin in the bed nucleus of the stria terminalis. Endocrinology 136:727-733.
87. 8-13 (LANT6)-related peptides in the basal ganglia of pigeons, turtles, and hamsters. J. Comp, Neurol. 257:453-476.
88. Reiner, A. and H. J. Karten (1985) Comparison of olfactory bulb projections in pigeons and turtles. Brain Behav. Evol. 27:11-27.
89. Reiner, A., H.J. Karten, and A.R. Solina (1983) Substance P: Localization within paleostriatal-tegmental pathways in the pigeon. Neuroscience 9:61-85.
90. Reiner, A., E.J. Karle, K.D. Anderson, and L. Medina (1994) Catecholaminergic perikarya and fibers in the avian nervous system. In W.J.A.J. Smeets and A. Reiner (eds): Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates. Cambridge UK: Cambridge University Press, pp. 135-181.
91. Roselli, C.E. (1991) Sex differences in androgen receptors and aromatase activity in microdissected regions of the rat brain. Endocrinology 128:1310-1316.
92. Roselli, C.E. and J.A. Resko (1993) Aromatase activity in the rat brain: Hormonal regulation and sex differences. J. Steroid Biochem. Mol. Biol. 44:499-508.
93. Roselli, C.E., L.E. Horton, and J.A. Resko (1985) Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinology 117:2471-2477.
94. Roselli, C.E., S.E. Abdelgadir, and J.A. Resko (1997) Regulation of aromatase gene expression in the adult rat brain. In G.C. Panzica and J. Balthazart (eds): Hormones, Brain, and Behavior. Brain Res. Bull. 44:351-357.
95. Sanghera, M.K., E.R. Simpson, M.J. Mcphaul, G. Kozlowski, A.J. Conley, and E.D. Lephart (1991) Immunocytochemical distribution of aromatase cytochrome P450 in the rat brain using peptide-generated polyclonal antibodies. Endocrinology 129:2834-2844.
96. Segovia, S. and A. Guillamon (1993) Sexual dimorphism in the vomeronasal pathway and sex differences in reproductive behaviors. Brain Res. Rev. 18:51-74.
97. Shen, P., B.A. Schlinger, A.T. Campagnoni, and A.P. Arnold (1995) An atlas of aromatase mRNA expression in the zebra finch brain. J. Comp. Neurol. 360:172-184.
98. Shinoda, K., M. Nagano, and Y. Osawa (1994) Neuronal aromatase expression in preoptic, striai, and amygdaloid regions during late prenatal and early postnatal development in the rat. J. Comp. Neurol. 343:113-129.
99. Simerly, R.B. and L.W. Swanson (1986) The organization of neural inputs to the medial preoptic nucleus of the rat. J. Comp. Neurol. 246:312-342.
100. Simerly, R.B. and L.W. Swanson (1998) Projections of the medial preoptic nucleus: A Phaseolus vulgaris leucoagglutinin anterograde tracttracing study in the rat. J. Comp. Neurol. 270:209-242.
101. Simerly, R.B., B.J. Young, M.A. Capozza, and L.W. Swanson (1989) Estrogen differentially regulates neuropeptide gene expression in a sexually dimorphic olfactory pathway. Proc. Natl. Acad. Sci. USA 86:4766-4770.
102. Stokes, T.M., C.M. Leonard, and F. Nottebohm (1974) The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J. Comp. Neurol. 156:337-374.
103. Takeo, T, M. Kudo, and Y. Sakuma (1995) Stria terminalis conveys a facilitatory estrogen effect on female rat lordosis reflex. Neurosci. Lett. 184:79-81.
104. Tsuruo, Y, K. Ishimura, H. Fujita, and Y. Osawa (1994) Immunohistochemical localization of aromatase-containing neurons in the rat brain during pre and postnatal development. Cell Tissue Res. 278:29-39.
105. Valcourt, R.J. and B.D. Sachs (1979) Penile reflexes and copulatory behavior in male rats following lesions in the bed nucleus of the stria terminalis. Brain Res. Bull. 4:131-133.
106. Van Furth, W.R., G. Wolterink, and J.M. Van Ree (1995) Regulation of masculine sexual behaviour: Involvement of brain opioids and dopamine. Brain Res. Rev. 21:162-184.
107. Van Leeuwen, F.W. and A.R. Caffé (1983) Vasopressin-immunoreactive cell bodies in the bed nucleus of the stria terminalis of the rat. Cell Tissue Res. 228:525-534.
108. Van Leeuwen, F.W., A.R. Gaffé, and G.J. De Vries (1985) Vasopressin cells in the bed nucleus of the stria terminalis of the rat: Sex differences and the influence of androgens. Brain Res. 325:391-394.
109. Veenman, C.L., J.M. Wild, and A. Reiner (1995) Organization of the avian "corticostriatal" projection system: A retrograde and anterograde pathway tracing study in pigeons. J. Comp. Neurol. 354:87-126.
110. Viglietti-Panzica, C. (1986) Immunohistochemical study of the distribution of vasotocin reacting neurons in avian diencephalon. J. Hirnforsch 27:559-566.
111. Viglietti-Panzica, C., G.C. Anselmetti, J. Balthazart, N. Aste, and G.C. Panzica (1992) Vasotocinergic innervation of the septal region in the Japanese quail: Sexual differences and the influence of testosterone. Cell Tissue Res. 267:261-265.
112. Viglietti-Panzica, C., N. Aste, J. Balthazart, and G.C. Panzica (1994) Vasotocinergic innervation of sexually dimorphic medial preoptic nucleus of the male Japanese quail: Influence of testosterone. Brain Res. 657:171-184.
113. Voorhuis, T.A.M. and E.R. De Kloet (1992) Immunoreactive vasotocin in the zebra finch brain (Taeniopigia guttata). Dev. Brain Res. 69:1-10.
114. Voorhuis, T.A.M., J.Z. Kiss, E.R. De Kloet, and D. De Wied (1988) Testosterone-sensitive vasotocin-immunoreactive cells and fibers in the canary brain. Brain Res. 442:139-146.
115. Wagner, C.K. and J.I. Morrell (1996) Distribution and steroid hormone regulation of aromatase mRNA expression in the forebrain of adult male and female rats: A cellular level analysis using in situ hybridization. J. Comp. Neurol. 370:71-84.
116. Walter, A., J.K. Mai, L. Lanta, and T. Gorcs (1991) Differential distribution of immunohistochemical markers in the bed nucleus of the stria terminalis in the human brain. J. Chem. Neuroanat. 4:281-298.
117. Wang, Z., W. Smith, D.E. Major, and G.J. De Vries (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.
118. 3H)-dihydrotestosterone. Neuroendocrinology 49:51-64.
119. Weller, K.L. and D.A. Smith (1982) Afferent connections to the bed nucleus of the stria terminalis. Brain Res. 232:255-270.
120. Wild, J.M., H.J. Karten, and B.J. Frost (1990) Projections of the parabrachial nucleus in the pigeon (Columbia livia). J. Comp. Neurol. 293:499-523.
121. Woodhams, P.L., G.W. Roberts, J.M. Polak, and T.J. Crow (1983) Distribution of neuropeptides in the limbic system of the rat: The bed nucleus of the stria terminalis, septum and preoptic area. Neuroscience 8:677-703.
122. Zeier, H. and H.J. Karten (1971) The archistriatum of the pigeon: Organization of afferent and efferent connections. Brain Res. 31:313-326.
123. Zhou, J.N., M.A. Hofman, L.J.G. Gooren, and D.F. Swaab (1995) A sex difference in the human brain and its relation to transsexuality. Nature 378:68-70.