Sexual dimorphism in numbers of vasotocin-immunoreactive neurons in brain areas associated with reproductive behaviors in the roughskin newt

General and Comparative Endocrinology

Volumn 117, Issue 2, 2000, Pages 281-298

  Moore, Frank L ^a   Richardson, Carla ^a   Lowry, Christopher A ^a  

^a OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROSTANOLONE; ARGIPRESTOCIN; ESTRADIOL; TESTOSTERONE;

AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; BRAIN; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; NEWT; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; RADIOIMMUNOASSAY; SEX DIFFERENCE; STRIA TERMINALIS;

EID: 0033961575     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1006/gcen.1999.7424     Document Type: Article

References (99)

1. Albers H. E., Liou S. Y., Ferris C. F. Testosterone alters the behavioral response of the medial preoptic-anterior hypothalamus to microinjection of arginine vasopressin in the hamster. Brain Res. 456:1988;382-386.
2. Albers H. E., Rawls S. Coordination of hamster lordosis and flank-marking behavior: Role of arginine vasopressin within the medial preoptic-anterior hypothalamus. Brain Res. Bull. 23:1989;105-109.
3. Baizer J. S., Whitney J. F., Bender D. B. Bilateral projections from the parabigeminal nucleus to the superior colliculus in monkey. Exp. Brain Res. 86:1991;467-470.
4. Bamshad M., Novak M. A., De Vries G. J. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster). Physiol. Behav. 56:1994;751-758.
5. Bluthe R. M., Dantzer R. Role of the vomeronasal system in vasopressinergic modulation of social recognition in rats. Brain Res. 604:1993;205-210.
6. Bons N. Immunocytochemical identification of the mesotocin- and vasotocin-producing systems in the brain of temperate and desert lizard species and their modifications by cold exposure. Gen. Comp. Endocrinol. 52:1983;56-66.
7. Boyd S. K. Effect of vasotocin on locomotor activity in bullfrogs varies with developmental stage and sex. Horm. Behav. 25:1991;57-69.
8. Boyd S. K. Sexual differences in hormonal control of release calls in bullfrogs. Horm. Behav. 26:1992;522-535.
9. Boyd S. K. Arginine vasotocin facilitation of advertisement calling and call phonotaxis in bullfrogs. Horm. Behav. 28:1994;232-240.
10. Boyd S. K., Moore F. L. Sexually dimorphic concentrations of arginine vasotocin in sensory regions of the amphibian brain. Brain Res. 588:1992;304-306.
11. Boyd S. K., Tyler C. J., De Vries G. J. Sexual dimorphism in the vasotocin system of the bullfrog (Rana catesbeiana). J. Comp. Neurol. 325:1992;313-325.
12. Brot M. D., De Vries G. J., Dorsa D. M. Local implants of testosterone metabolites regulate vasopressin mRNA in sexually dimorphic nuclei of the rat brain. Peptides. 14:1993;933-940.
13. Bruce L. L., Neary T. J. The limbic system of tetrapods: A comparative analysis of cortical and amygdalar populations. Brain Behav. Evol. 46:1995;224-234.
14. Caffé A. R., van Leeuwen F. W. Vasopressin-immunoreactive cells in the dorsomedial hypothalamic region, medial amygdaloid nucleus and locus coeruleus of the rat. Cell Tissue Res. 233:1983;23-33.
15. Carter C. S., DeVries A. C., Getz L. L. Physiological substrates of monogamy: The prairie vole model. Neurosc. Biobehav. Rev. 19:1995;303-314.
16. Castel M., Morris J. F. The neurophysin-containing innervation of the forebrain of the mouse. Neuroscience. 24:1988;937-966.
17. Chu J., Marler C. A., Wilczynski W. The effects of arginine vasotocin on the calling behavior of male cricket frogs in changing social contexts. Horm. Behav. 34:1998;248-261.
18. De Vries G. J. Sex differences in neurotransmitter systems. J. Neuroendocrinol. 2:1990;1-13.
19. De Vries G. J. Studying neurotransmitter systems to understand development and function of sex differences in the brain: The case of vasopressin. Micevych P., Hammer R. P. Neurobiological Effects of Sex Steroid Hormones. 1994;Cambridge Univ. Press, Cambridge.
20. De Vries G. J., Boyle P. A. Double duty for sex differences in the brain. Behav. Brain Res. 92:1998;205-213.
21. De Vries G. J., Buijs R. M., van Leeuwen F. W., Caffé A. R., Swaab D. F. The vasopressinergic innervation of the brain in normal and castrated rats. J. Comp. Neurol. 233:1985;236-254.
22. De Vries G. J., Miller M. A. Anatomy and function of extrahypothalamic vasopressin systems in the brain. Urban I. J. A., Burbach J. P. H., De Wied D. Progress in Brain Research. 1998;3-20 Elsevier Science, New York.
23. De Vries G. J., Wang Z., Bullock N. A., Numan S. 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. 14:1994;1789-1794.
24. Deviche P., Moore F. L. Steroidal control of sexual behavior in the rough-skinned newt (Taricha granulosa): Effect of testosterone, estradiol, and dihydrotestosterone. Horm. Behav. 22:1988;26-34.
25. Deviche P., Propper C. R., Moore F. L. Neuroendocrine, behavioral, and morphological changes associated with the termination of the reproductive period in a natural population of male rough-skinned newts (Taricha granulosa). Horm. Behav. 24:1990;284-300.
26. De Vries G. J., Duetz W., Buijs R. M., Van Heerikhuize J., Vreeburg J. T. M. Effects of androgens and estrogens on the vasopressin and oxytocin innervation of the adult rat brain. Brain Res. 399:1986;296-302.
27. Di Michele S., Ericson M., Sillen U., Engel J. A., Soderpalm B. The role of catecholamines in desmopressin induced locomotor stimulation. J. Neural Transm. 105:1998;1103-1115.
28. Diakow C. Hormonal basis for breeding behavior in female frogs: Vasotocin inhibits the release call of Rana pipiens. Science. 199:1978;1456-1457.
29. Dubois-Dauphin M., Barberis C., De Bilbao F. Vasopressin receptors in the mouse (Mus musculus) brain: Sex-related expression in the medial preoptic area and hypothalamus. Brain Res. 743:1996;32-39.
30. Dubois-Dauphin M., Tribollet E., Dreifuss J. J. Distribution of neurohypophysial peptides in the guinea pig brain. I. An immunocytochemical study of the vasopressin-related glycopeptide. 496:1989;45-65.
31. Emerson S. R., Hess D. L. The role of androgens in opportunistic breeding tropical frogs. Gen. Comp. Endocrinol. 103:1996;220-230.
32. Grober M. S., Sunobe T. Serial adult sex change involves rapid and reversible changes in forebrain neurochemistry. NeuroReport. 7:1996;2945-2949.
33. Fernández-Llebrez P. J. P., Nadales A. E., Cifuentes M., Grondona J. M., Mancera J. M., Rodriquez E. M. Immunocytochemical study of the hypothalamic magnocellular neurosecretory nuclei of the snake Natrix maura and the turtle Mauremys caspica. Cell Tissue Res. 253:1988;435-445.
34. Ferris C. F., Delville Y. Vasopressin and serotonin interactions in the control of agonistic behavior. Psychoneuroendocrinology. 19:1994;593-601.
35. Fliers E., Guldenaar S. E. F., Wal N., Swaab D. F. Extrahypothalamic vasopressin and oxytocin in the human brain; presence of vasopressin cells in the bed nucleus of the stria terminalis. Brain Res. 375:1986;363-367.
36. Gobbetti A., Zerani M., Carnevali O., Botte V. Prostaglandin F2α in female water frog, Rana esculenta: Plasma levels during the annual cycle and effects of exogenous PGF2? on circulating sex hormones. Gen. Comp. Endocrinol. 80:1990;175-180.
37. González A., Smeets W. J. A. J. Comparative analysis of the vasotocinergic and mesotocinergic cells and fibers in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii. J. Comp. Neurol. 315:1992;53-73.
38. Goodson J. L. Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm. Behav. 34:1998a;67-77.
39. Goodson J. L. Vasotocin and vasoactive intestinal polypeptide modulate aggression in a territorial songbird, the violet-eared waxbill (Estrildidae: Uraeginthus granatina). Gen. Comp. Endocrinol. 111:1998b;233-244.
40. Goodson J. L., Adkins-Regan E. Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata). J. Neuroendocrinol. 11:1999;19-25.
41. Herrick C. J. The Brain of the Tiger Salamander Ambystoma tigrinum. 1948;Univ. of Chicago Press, Chicago.
42. Insel T. R., O'Brien D. J., Leckman J. F. Oxytocin, vasopressin, and autism: Is there a connection. Biol. Psychiatry. 45:1999;145-157.
43. Johnston J. B. Further contributions to the study of the evolution of the forebrain. J. Comp. Neurol. 35:1923;337-481.
44. Jurkevich A., Barth S. W., Aste N., Panzica G. C., Grossmann R. Intracerebral sex differences in the vasotocin system in birds: Possible implication in behavioral and autonomic functions. Horm. Behav. 30:1996;673-681.
45. Jurkevich A., Barth S. W., Kuenzel W. J., Kohler A., Grossmann R. Development of sexually dimorphic vasotocinergic system in the bed nucleus of stria terminalis in chickens. J. Comp. Neurol. 408:1999;46-60.
46. Kihlstrom J. E., Danninge I. Neurohypophysial hormones and sexual behavior in males of the domestic fowl (Gallus domesticus L.) and the pigeon (Columba livia Gmel.). Gen. Comp. Endocrinol. 18:1972;115-120.
47. Kiss J. Z., Voorhuis T. A. M., van Eekelen J. A. M., de Kloet E. R., deWied D. Organization of vasotocin-immunoreactive cells and fibers in the canary brain. J. Comp. Neurol. 263:1987;347-364.
48. Lowry C. A., Renner K. J., Moore F. L. Catecholamines and indoleamines in the central nervous system of a urodele amphibian: A microdissection study with emphasis on the distribution of epinephrine. Brain Behav. Evol. 48:1996;70-93.
49. Lowry C. A., Richardson C. F., Zoeller R. T., Miller L. J., Muske L. E., Moore F. L. Neuroanatomical distribution of vasotocin in a urodele amphibian (Taricha granulosa) revealed by immunohistochemical and in situ hybridization techniques. J. Comp. Neurol. 385:1997;43-70.
50. Malacarne G., Giacoma C. Effects of lesions to the rostral preoptic area on courtship behaviour in the male crested newt Triturus cristatus carnifex (Laur.). Monit. Zool. Ital. 14:1980;9-17.
51. Marler C. A., Boyd S. K., Wilczynski W. Forebrain arginine vasotocin correlates of alternative mating strategies in cricket frogs. Horm. Behav. 36:1999;53-61.
52. Marler C. A., Chu J., Wilczynski W. Arginine vasotocin injection increases probability of calling in cricket frogs, but causes call changes characteristic of less aggressive males. Horm. Behav. 29:1995;554-570.
53. Mathieson W. B. Development of arginine vasotocin innervation in two species of anuran amphibian - Rana catesbeiana and Rana sylvatica. Histochem. Cell Biol. 105:1996;305-318.
54. Metzger D., Alescio-Lautier B., Bosler O., Devigne C. Effect of changes in the intrahippocampal vasopressin on memory retrieval and relearning. Behav. Neural. Biol. 59:1993;29-48.
55. Miller M. A., De Vries G. J., Al-Shamma H. A., Dorsa D. M. Decline of vasopressin immunoreactivity and mRNA levels in the bed nucleus of the stria terminalis following castration. J. Neurosci. 12:1992;2881-2887.
56. Moore F. L. Differential effects of testosterone plus dihydrostestosterone on male courtship of castrated newts. Taricha granulosa. Horm. Behav. 11:1978;202-208.
57. Moore F. L. Evolutionary precedents for behavioral actions of oxytocin and vasopressin. Ann. N.Y. Acad. Sci. 652:1992;156-165.
58. Moore F. L., Lowry C. A. Comparative neuroanatomy of vasotocin and vasopressin in amphibians and other vertebrates. Comp. Biochem. Physiol. C. 119:1998;251-260.
59. Moore F. L., Lowry C. A., Rose J. D. Steroid-neuropeptide interactions and the control of reproductive behaviors. Psychoneuroendocrinology. 19:1994;581-592.
60. Moore F. L., McCormack C., Swanson L. Induced ovulation: Effects of sexual behavior and insemination on ovulation and progesterone levels in Taricha granulosa. Gen. Comp. Endocrinol. 39:1979;262-269.
61. Moore F. L., Miller L. J. Arginine vasotocin induces sexual behavior of newts by acting on cells in the brain. Peptides. 4:1983;97-102.
62. Moore F. L., Muller C. H., Specker J. L. Origin and regulation of plasma dihydrotestosterone and testosterone in the rough-skinned newt, Taricha granulosa. Gen. Comp. Endocrinol. 38:1979;451-456.
63. Moore F. L., Wood R. E., Boyd S. K. Sex steroids and vasotocin interact in a female amphibian (Taricha granulosa) to elicit female-like egg-laying behavior or male-like courtship. Horm. Behav. 26:1992;156-166.
64. Moore F. L., Zoeller R. T. Endocrine control of amphibian sexual behavior: Evidence for a neurohormone-androgen interaction. Horm. Behav. 13:1979;207-213.
65. Nakada T., Soh T., Shiota T., Tanaka K. Studies on the role of arginine vasotocin in relation to oviposition in laying hens. Jpn. Poult. Sci. 31:1994;358-362.
66. Northcutt R. G., Kicliter E. Organization of the amphibian telencephalon. Eddesson S. O. E. Comparative Neurology of the Telencephalon. 1980;203-255 Plenum, New York.
67. Ota Y., Ando H., Ueda H., Urano A. Differences in seasonal expression of neurohypophysial hormone genes in ordinary and precocious male masu salmon. Gen. Comp. Endocrinol. 116:1999;40-48.
68. Ota Y., Ando H., Ueda H., Urano A. Seasonal changes in expression of neurohypophysial hormone genes in the preoptic nucleus of immature female masu salmon. Gen. Comp. Endocrinol. 116:1999;31-39.
69. Panzica G. C., Castagna C., Viglietti-Panzica C., Russo C., Tlemcani O., Balthazart J. Organizational effects of estrogens on brain vasotocin and sexual behavior in quail. J. Neurobiol. 37:1998;684-699.
70. Panzica G. C., Garcia Ojeda E., Viglietti Panzica C., Thompson N. E., Ottinger M. A. Testosterone effects of vasotocinergic innervation of sexually dimorphic medial preoptic nucleus and lateral septum during aging in male quail. Brain Res. 712:1996;190-198.
71. Panzica G. C., Viglietti-Panzica C., Balthazart J. The sexually dimorphic medial preoptic nucleus of quail: A key brain area mediating steroid action on male sexual behavior. Frontiers Neuroendocrinol. 17:1996;51-125.
72. Penna M., Capranica R. R., Somers J. J. Hormone-induced vocal behavior and midbrain auditory sensitivity in the green treefrog, Hyla cinerea. J. Comp Physiol A. 170:1991;73-82.
73. Propper C. R. Courtship in the rough-skinned newt Taricha granulosa. Anim. Behav. 41:1991;547-554.
74. Propper C. R., Dixon T. B. Differential effects of arginine vasotocin and gonadotropin-releasing hormone on sexual behaviors in an anuran amphibian. Horm. Behav. 32:1997;99-104.
75. Propper C. R., Jones R. E., Lopez K. H. Distribution of arginine vasotocin in the brain of the lizard, Anolis carolinensis. Cell Tissue Res. 267:1992;391-398.
76. Propper C. R., Moore F. L. Effects of courtship on brain gonadotropin hormone-releasing hormone and plasma steroid concentrations in a female amphibian (Taricha granulosa). Gen. Comp. Endocrinol. 81:1991;304-312.
77. Resko J. A., Ellinwood W. E., Pasztor L. M., Buhl A. E. Sex steroids in the umbilical circulation of the fetal rhesus monkeys from the time of gonadal differentiation. J. Clin. Endocrinol. Metab. 50:1980;900-905.
78. Resko J. A., Ploem J. G., Stadelman H. L. Estrogens in fetal and maternal plasma of the rhesus monkey. Endocrinology. 97:1975;425-430.
79. Rose J. D., Moore F. L. A neurobehavioral model for rapid actions of corticosterone on sensorimotor integration. Steroids. 64:1999;92-99.
80. Smeets W. J. A. J., Sevensma J. J., Jonker A. J., Blähser S. Comparative analysis of vasotocin-like immunoreactivity in the brain of the turtle Pseudemys scripta elegans and the snake Python regius. Brain Behav. Evol. 35:1983;11-24.
81. Sodersten P., Henning M., Melin P., Ludlin S. Vasopressin alters female sexual behaviour by acting on the brain independently of alterations in blood pressure. Nature. 301:1983;608-610.
82. Sofroniew, M. V.1985. Vasopressin, oxytocin and their related neurophysins. InHandbook of Chemical NeuroanatomyA. Bjorklund and T. Hokfeld, Eds., Vol. 4, GABA and Neuropeptides in the CNS, Part I, pp. 93-165. Elsevier, Amsterdam.
83. Specker J. L., Moore F. L. Annual cycle of plasma androgens and testicular composition in the rough-skinned newt, Taricha granulosa. Gen. Comp. Endocrinol. 42:1980;297-303.
84. Stoll C. J., Voorn P. The distribution of hypothalamic and extrahypothalamic vasotocinergic cells and fibers in the brain of a lizard, Gekko gecko: Presence of a sex difference. J. Comp. Neurol. 239:1985;193-204.
85. Takami S., Urano A. The volume of the toad medial amygdala-anterior preoptic complex is sexually dimorphic and seasonally variable. Neurosci. Lett. 44:1984;253-258.
86. Thepen T., Voorn P., Stoll C. J., Sluiter A. A., Pool C. W. Mesotocin and vasotocin in the brain of the lizard Gekko gecko: An immunocytochemical study. Cell Tissue Res. 250:1987;649-656.
87. Tito M. B., Hoover M. A., Mingo A. M., Boyd S. K. Vasotocin maintains multiple call types in the gray treefrog, Hyla versicolor. Horm. Behav. 36:1999;166-175.
88. Tobet S. A., Hanna I. K. Ontogeny of sex differences in the mammalian hypothalamus and preoptic area. Cell Mol. Neurobiol. 17:1997;565-601.
89. Urano A. Neuroendocrine control of anuran anterior preoptic neurons and initiation of mating behavior. Zool. Sci. 5:1988;925-937.
90. van Leeuwen F., Caffé R. Vasopressin-immunoreactive cell bodies in the bed nucleus of the stria terminalis of the rat. Cell Tissue Res. 228:1983;525-534.
91. van Leeuwen F. W., Caffé R., van der Sluis P. J., Sluiter A. A., van der Woude T. P., Seidah N. G., Chrétien M. Propressophysin is present in neurons at multiple sites in Wistar and homozygous Brattleboro rat brain. Brain Res. 379:1986;171-175.
92. Vigliette-Panzica C., Aste N., Balthazart J., Panzica G. C. Vasotocinergic innervation of sexually dimorphic medial preoptic nucleus of the male Japanese quail: Influence of testosterone. Brain Res. 657:1994;171-184.
93. Voorhuis T. A. M., de Kloet E. R. Immunoreactive vasotocin in the zebra finch brain (Taeniopygia guttata). Dev. Brain Res. 69:1992;1-10.
94. Voorhuis T. A. M., deKloet E. R., deWied D. Effect of a vasotocin analog on singing behavior in the canary. Horm. Behav. 25:1991;549-559.
95. Wang Z., Bullock N. A., De Vries G. J. Sexual differentiation of vasopressin projections of the bed nucleus of the stria terminalis and medial amygdaloid nucleus in rats. Endocrinology. 132:1993;2299-2306.
96. Wiggers W., Roth G. Anatomy, neurophysiology and functional aspects of the nucleus isthmi in salamanders of the family Plethodontidae. Behav. Physiol. 169:1991;165-176.
97. Zerani M., Amabili F., Gobbetti A. Plasma testosterone and 17β-estradiol concentrations, and aromatase activity, during courtship in male Triturus carnifex. Horm. Behav. 26:1992;56-61.
98. Zoeller R. T., Moore F. L. Duration of androgen treatment modifies behavioral response to arginine vasotocin in Taricha granulosa. Horm. Behav. 16:1982;23-30.
99. Zoeller R. T., Moore F. L. Brain arginine vasotocin concentrations related to sexual behaviors and hydromineral balance in an amphibian. Horm. Behav. 22:1988;66-75.