Cryptic regulation of vasotocin neuronal activity but not anatomy by sex steroids and social stimuli in opportunistic desert finches

Brain, Behavior and Evolution

Volumn 75, Issue 1, 2010, Pages 71-84

  Kabelik, David ^a   Morrison, Jenilee A ^a   Goodson, James L ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Bed nucleus of the stria terminalis; Bird; C fos; Estradiol; Lateral septum; Seasonality; Testosterone; Vasopressin; Vasotocin; Zebra finch

Indexed keywords

ANDROGEN RECEPTOR; ANTIANDROGEN; ARGIPRESTOCIN; AROMATASE INHIBITOR; ESTRADIOL; FLUTAMIDE; PROTEIN C FOS; SEX HORMONE;

ANIMAL; ARTICLE; BRAIN; BRAIN MAPPING; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; FINCH; GENETICS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; NERVE CELL; PHYSIOLOGY; SEPTUM NUCLEUS; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT; SOCIAL BEHAVIOR; SPECIES DIFFERENCE;

ANDROGEN ANTAGONISTS; ANIMALS; AROMATASE INHIBITORS; BRAIN; BRAIN MAPPING; ESTRADIOL; FEMALE; FINCHES; FLUTAMIDE; GONADAL STEROID HORMONES; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; PAIR BOND; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, ANDROGEN; SEPTAL NUCLEI; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; SPECIES SPECIFICITY; VASOTOCIN;

AVES; ESTRILDIDAE; FRINGILLIDAE; MAMMALIA; TAENIOPYGIA GUTTATA; VERTEBRATA;

EID: 77950225673     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000297522     Document Type: Article

References (77)

1. Auger CJ, De Vries GJ (2002) Progestin receptor immunoreactivity within steroid-responsive vasopressin-immunoreactive cells in the male and female rat brain. J Neuroendocrinol 14: 561-567.
2. Axelson JF, Leeuwen FW (1990) Differential localization of estrogen receptors in various vasopressin synthesizing nuclei of the rat brain. J Neuroendocrinol 2: 209-216.
3. Bentley GE, Spar BD, MacDougall-Shackleton SA, Hahn TP, Ball GF (2000) Photoperiodic regulation of the reproductive axis in male zebra finches, Taeniopygia guttata . Gen Comp Endocrinol 117: 449-455.
4. Bester-Meredith JK, Marler CA (2001) Vasopressin and aggression in cross-fostered California mice (Peromyscus californicus) and white-footed mice (Peromyscus leucopus) . Horm Behav 40: 51-64.
5. Bosch OJ, Neumann ID (2008) Brain vasopressin is an important regulator of maternal behavior independent of dams' trait anxiety. Proc Natl Acad Sci USA 105: 17139-17144.
6. Boyd SK (1994) Gonadal steroid modulation of vasotocin concentrations in the bullfrog brain. Neuroendocrinology 60: 150-156.
7. Buijs RM, Pevet P, Masson Pevet M, Pool CW, De Vries GJ, Canguilhem B, Vivien-Roels B (1986) Seasonal variation in vasopressin innervation in the brain of the European hamster Cricetus cricetus . Brain Res 371: 193-196.
8. Caldwell HK, Lee H, Macbeth AH, Young WS 3rd (2008) Vasopressin: Behavioral roles of an 'original' neuropeptide. Prog Neurobiol 84: 1-24.
9. Carter CS, Grippo AJ, Pournajafi-Nazarloo H, Ruscio MG, Porges SW (2008) Oxytocin, vasopressin and sociality. Prog Brain Res 170: 331-336.
10. Chandola-Saklani A, Thapliyal A, Negi K, Diyundi SC, Choudhary B (2004) Daily increments of light hours near vernal equinox synchronize circannual testicular cycle of tropical spotted munia. Chronobiol Int 21: 553-569.
11. Chaturvedi CM, Prasad SK (1991) Timed daily injections of neurotransmitter precursors alter the gonad and body weights of spotted munia, Lonchura punctulata , maintained under short daily photoperiods. J Exp Zool 260: 194-201.
12. Clayton NS (1990) Mate choice and pair formation in Timor and Australian mainland zebra finches. Anim Behav 39: 474-480.
13. Crenshaw BJ, De Vries GJ, Yahr P (1992) Vasopressin innervation of sexually dimorphic structures of the gerbil forebrain under various hormonal conditions. J Comp Neurol 322: 589-598.
14. Cynx J (2001) Effects of humidity on reproductive behavior in male and female zebra finches (Taeniopygia guttata) . J Comp Psychol 115: 196-200.
15. De Vries GJ, Boyle PA (1998) Double duty for sex differences in the brain. Behav Brain Res 92: 205-213.
16. De Vries GJ, Panzica GC (2006) Sexual differentiation of central vasopressin and vasotocin systems in vertebrates: different mechanisms, similar endpoints. Neuroscience 138: 947-955.
17. De Vries GJ, Buijs RM, Sluiter AA (1984) Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain. Brain Res 298: 141-145.
18. De Vries 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.
19. De Vries GJ, Duetz W, Buijs RM, Van Heerikhuize J, Vreeburg JTM (1986) Effects of androgens and estrogens on the vasopressin and oxytocin innervation of the adult rat brain. Brain Res 399: 296-302.
20. 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.
21. Donaldson ZR, Young LJ (2009) Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322: 900-904.
22. Dubois-Dauphin M, Theler JM, Ouarour A, Pevet P, Barberis C, Dreifuss JJ (1994) Regional differences in testosterone effects on vasopressin receptors and on vasopressin immunoreactivity in intact and castrated Siberian hamsters. Brain Res 638: 267-276.
23. Frazier CRM, Trainor BC, Cravens CJ, Whitney TK, Marler CA (2006) Paternal behavior influences development of aggression and vasopressin expression in male California mouse offspring. Horm Behav 50: 699-707.
24. Goodson JL (2008) Nonapeptides and the evolutionary patterning of sociality. Prog Brain Res 170: 3-15.
25. Goodson JL, Adkins-Regan E (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.
26. Goodson JL, Bass AH (2001) Social behavior functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Brain Res Rev 35: 246-265.
27. Goodson JL, Evans AK (2004) Neural responses to territorial challenge and nonsocial stress in male song sparrows: segregation, integration, and modulation by a vasopressin V 1 antagonist. Horm Behav 46: 371-381.
28. Goodson JL, Kabelik D (2009) Dynamic limbic networks and social diversity in vertebrates: from neural context to neuromodulatory patterning. Front Neuroendocrinol 30: 429-441.
29. Goodson JL, Wang Y (2006) Valence-sensitive neurons exhibit divergent functional profiles in gregarious and asocial species. Proc Natl Acad Sci USA 103: 17013-17017.
30. Goodson JL, Evans AK, Lindberg L (2004a) Chemoarchitectonic subdivisions of the songbird septum and a comparative overview of septum chemical anatomy in jawed vertebrates. J Comp Neurol 473: 293-314.
31. Goodson JL, Evans AK, Lindberg L, Allen CD (2005b) Neuro-evolutionary patterning of sociality. Proc Biol Sci 272: 227-235.
32. Goodson JL, Evans AK, Soma KK (2005a) Neural responses to aggressive challenge correlate with behavior in nonbreeding sparrows. Neuroreport 16: 1719-1723.
33. Goodson JL, Evans AK, Wang Y (2006) Neuropeptide binding reflects convergent and divergent evolution in species-typical group sizes. Horm Behav 50: 223-236.
34. Goodson JL, Kabelik D, Schrock SE (2009a) Dynamic neuromodulation of aggression by vasotocin: influence of social context and social phenotype in territorial songbirds. Biol Lett 5: 554-556.
35. Goodson JL, Lindberg L, Johnson P (2004b) Effects of central vasotocin and mesotocin manipulations on social behavior in male and female zebra finches. Horm Behav 45: 136-143.
36. Goodson JL, Rinaldi J, Kelly AM (2009b) Vasotocin neurons in the bed nucleus of the stria terminalis preferentially process social information and exhibit properties that dichotomize courting and non-courting phenotypes. Horm Behav 55: 197-202.
37. Goodwin D (1982) Estrildid Finches of the World. Ithaca, NY: Cornell University Press.
38. Hahn TP, MacDougall-Shackleton SA (2008) Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Philos Trans R Soc Lond B Biol Sci 363: 267-286.
39. Hahn TP, Watts HE, Cornelius JM, Brazeal KR, MacDougall-Shackleton SA (2009) Evolution of environmental cue response mechanisms: Adaptive variation in photorefractoriness. Gen Comp Endocrinol 163: 193-200.
40. Immelmann K (1965) Australian finches in bush and aviary. Sydney and London: Angus and Robertson.
41. Kabelik D, Kelly AM, Goodson JL (2010) Dopaminergic regulation of mate competition aggression and aromatase-Fos colocalization in vasotocin neurons. Neuropharmacology 58: 862-866.
42. Kabelik D, Klatt JD, Kingsbury MA, Goodson JL (2009) Endogenous vasotocin exerts context-dependent behavioral effects in a seminaturalistic colony environment. Horm Behav 56: 101-107.
43. Kabelik D, Weiss SL, Moore MC (2008) Arginine vasotocin (AVT) immunoreactivity relates to testosterone but not territorial aggression in the tree lizard, Urosaurus ornatus . Brain Behav Evol 72: 283-294.
44. Kimura T, Okanoya K, Wada M (1999) Effect of testosterone on the distribution of vasotocin immunoreactivity in the brain of the zebra finch, Taeniopygia guttata castanotis . Life Sci 65: 1663-1670.
45. Lakhdar-Ghazal N, Dubois Dauphin M, Hermes MLHJ, Buijs RM, Bengelloun WA, Pevet P (1995) Vasopressin in the brain of a desert hibernator, the Jerboa (Jaculus orientalis) : Presence of sexual dimorphism and seasonal variation. J Comp Neurol 358: 499-517.
46. Lee DW, Fernando G, Peterson RS, Allen TA, Schlinger BA (2007) Estrogen mediation of injury-induced cell birth in neuroproliferative regions of the adult zebra finch brain. Dev Neurobiol 67: 1107-1117.
47. Lim MM, Young LJ (2006) Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Horm Behav 50: 506-517.
48. Marler CA, Bester-Meredith JK, Trainor BC (2003) Paternal behavior and aggression: Endocrine mechanisms and nongenomic transmission of behavior. In: Advances in the Study of Behavior (Slater PJB, Rosenblatt JS, Snowdon CT, Roper TJ, eds), vol 32, pp 263- 323. New York: Academic Press.
49. Meddle SL, Foidart A, Wingfield JC, Ramenofskyand M, Balthazart J (1999) Effects of sexual interactions with a male on fos-like immunoreactivity in the female quail brain. J Neuroendocrinol 11: 771-784.
50. Miller MA, De Vries GJ, al-Shamma HA, Dorsa DM (1992) Decline of vasopressin immunoreactivity and mRNA levels in the bed nucleus of the stria terminalis following castration. J Neurosci 12: 2881-2887.
51. Miller MA, Urban JH, Dorsa DM (1989) Steroid dependency of vasopressin neurons in the bed nucleus of the stria terminalis by in situ hybridization. Endocrinology 125: 2335-2340.
52. Moore FL, Richardson C, Lowry CA (2000) Sexual dimorphism in numbers of vasotocinimmunoreactive neurons in brain areas associated with reproductive behaviors in the roughskin newt. Gen Comp Endocrinol 117: 281-298.
53. Moore MC (1986) Elevated testosterone levels during nonbreeding-season territoriality in a fall-breeding lizard, Sceloporus jarrovi . J Comp Physiol A 158: 159-163.
54. Morton S (2009) Rain and grass: lessons in how to be a zebra finch. In: Boom and Bust: Bird Stories for a Dry Country (Robin L, Heinsohn R, Joseph L, eds), pp 45-74. Collingwood, Victoria: CSIRO.
55. Panzica GC, Aste N, Castagna C, Viglietti-Panzica C, Balthazart J (2001) Steroid-induced plasticity in the sexually dimorphic vasotocinergic innervation of the avian brain: behavioral implications. Brain Res Brain Res Rev 37: 178-200.
56. Perfito N, Kwong JM, Bentley GE, Hau M (2008) Cue hierarchies and testicular development: is food a more potent stimulus than day length in an opportunistic breeder (Taeniopygia g. guttata) ? Horm Behav 53: 567-572.
57. Perfito N, Zann RA, Bentley GE, Hau M (2007) Opportunism at work: habitat predictability affects reproductive readiness in free-living zebra finches. Funct Ecol 21: 291-301.
58. Plumari L, Plateroti S, Deviche P, Panzica GC (2004) Region-specific testosterone modulation of the vasotocin-immunoreactive system in male dark-eyed junco, Junco hyemalis . Brain Res 999: 1-8.
59. Rasri K, Mason P, Govitrapong P, Pevet P, Klosen P (2008) Testosterone-driven seasonal regulation of vasopressin and galanin in the bed nucleus of the stria terminalis of the Djungarian hamster (Phodopus sungorus) . Neuroscience 157: 174-187.
60. Scordalakes EM, Rissman EF (2004) Aggression and arginine vasopressin immunoreactivity regulation by androgen receptor and estrogen receptor alpha. Genes Brain Behav 3: 20-26.
61. Sikdar M, Kar A, Prakash P (1992) Role of humidity in the seasonal reproduction of male spotted munia, Lonchura punctulata . J Exp Zool 264: 82-84.
62. Skead DM (1975) Ecological studies of four estrildines in the central Transvaal. Ostrich (suppl)11: 1-55.
63. Small TW, Moore IT (2009) Seasonal neuroplasticity of the song control system in tropical, flexibly, and opportunistically breeding birds. Gen Comp Endocrinol 163: 135-141.
64. Soma KK, Sullivan K, Wingfield J (1999) Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season. Gen Comp Endocrinol 115: 442-453.
65. Szot P, Dorsa DM (1994) Expression of cytoplasmic and nuclear vasopressin RNA following castration and testosterone replacement: evidence for transcriptional regulation. Mol Cell Neurosci 5: 1-10.
66. van Leeuwen FW, Caffe AR, De Vries GJ (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.
67. Veenema AH, Neumann ID (2008) Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog Brain Res 170: 261-276.
68. Viglietti-Panzica C, Anselmetti GC, Balthazart J, Aste N, Panzica GC (1992) Vasotocinergic innervation of the septal region in the Japanese quail: sexual differences and the influence of testosterone. Cell Tissue Res 267: 261-265.
69. Viglietti-Panzica C, Balthazart J, Plumari L, Fratesi S, Absil P, Panzica GC (2001) Estradiol mediates effects of testosterone on vasotocin immunoreactivity in the adult quail brain. Horm Behav 40: 445-461.
70. Voorhuis TA, de Kloet ER (1992) Immunoreactive vasotocin in the zebra finch brain (Taeniopygia guttata) . Brain Res Dev Brain Res 69: 1-10.
71. Voorhuis TAM, Kiss JZ, de Kloet ER, de Wied D (1988) Testosterone- sensitive vasotocin-immunoreactive cells and fibers in the canary brain. Brain Res 442: 139-146.
72. Wang Z, De Vries GJ (1993) Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster) . Brain Res 631: 156-160.
73. 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.
74. Wingfield JC (2008) Organization of vertebrate annual cycles: implications for control mechanisms. Philos Trans R Soc Lond B Biol Sci 363: 425-441.
75. Zann R (1994) Reproduction in a zebra finch colony in south-eastern Australia: the significance of monogamy, precocial breeding and multiple broods in a highly mobile species. Emu 94: 285-299.
76. Zann RA (1996) The Zebra Finch: a synthesis of field and laboratory studies. Oxford, UK: Oxford University Press.
77. Zhou L, Blaustein JD, De Vries GJ (1994) Distribution of androgen receptor immunoreactivity in vasopressin- and oxytocin-immunoreactive neurons in the male rat brain. Endocrinology 134: 2622-2627.