Sex and seasonal differences in morphology of limbic forebrain nuclei in the green anole lizard

Brain Research

Volumn 1227, Issue , 2008, Pages 68-75

  Beck, Laurel A ^a   O'Bryant, Erin L ^a   Wade, Juli S ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Lizard; Preoptic area; Seasonal plasticity; Sexual dimorphism; Ventromedial amygdala; Ventromedial hypothalamus

Indexed keywords

STEROID HORMONE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN NUCLEUS; BRAIN REGION; BRAIN SIZE; BREEDING; CELL COUNT; CELL SIZE; COMPARATIVE STUDY; FEMALE; FOREBRAIN; LIMBIC CORTEX; LIZARD; MALE; MASCULINITY; MORPHOLOGY; NONHUMAN; PERIKARYON; PREOPTIC AREA; PRIORITY JOURNAL; SEASONAL VARIATION; SEX DIFFERENCE; SEXUAL BEHAVIOR; ZONA INCERTA;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; FEMALE; LIMBIC SYSTEM; LIZARDS; MALE; NEURONS; PREGNANCY; PREOPTIC AREA; PROSENCEPHALON; REPRODUCTION; SEASONS; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; VENTROMEDIAL HYPOTHALAMIC NUCLEUS;

ANIMALIA; ANOLIS CAROLINENSIS; SQUAMATA;

EID: 48949107090     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.06.021     Document Type: Article

References (84)

1. Absil P., Pinxten R., Balthazart J., and Eens M. Effect of age and testosterone on autumnal neurogenesis in male European starlings (Sturnus vulgaris). Behav. Brain Res. 143 (2003) 15-30
2. Adkins-Regan E., and Watson J.T. Sexual dimorphism in the avian brain is not limited to the song system of songbirds: a morphometric analysis of the brain of the quail (Coturnix japonica). Brain Res. 514 (1990) 320-326
3. Alvarez-Buylla A., Theelen M., and Nottebohm F. Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 8722-8726
4. Alvarez-Borda B., and Nottebohm F. Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain. J. Neurosci. 22 (2002) 8684-8690
5. Ball G.F., Auger C.J., Bernard D.J., Charlier T.D., Sartor J.J., Riters L.V., and Balthazart J. Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann. N. Y. Acad. Sci. 1016 (2004) 586-610
6. Balthazart J., and Surlemont C. Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail POA. Brain Res. Bull. 25 (1990) 7-14
7. Baum M.J. Neuroendocrinology of sexual behavior in the male. In: Becker J.B., Breedlove S.M., Crews D., and McCarthy M.M. (Eds). Behavioral Endocrinology. 2nd ed. (2002), MIT Press, Cambridge, MA 153-203
8. Bentley G.E., Van't Hof T.J., and Ball G.F. Seasonal neuroplasticity in the songbird telencephalon: a role for melatonin. Proc. Natl. Acad. Sci. U S A. 96 (1999) 4674-4679
9. Bernier P.J., Bedard A., Vinet J., Levesque M., and Parent A. Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc. Natl. Acad. Sci. U S A. 99 (2002) 11464-11469
10. Bloch G.J., and Gorski R.A. Cytoarchitectonic analysis of the SDN-POA of the intact and gonadectomized rat. J. Comp. Neurol. 275 (1988) 604-612
11. Bonsall R.W., Clancy A.N., and Michael R.P. Effects of the nonsteroidal inhibitor, fadrozole, on sexual behavior in male rats. Horm. Behav. 20 (1992) 240-254
12. Brenowitz E.A., Baptista L.F., Lent K., and Wingfield J.C. Seasonal plasticity of the song control system in wild Nuttall's white-crowned sparrows. J. Neurobiol. 34 (1998) 69-82
13. Bruce L.L., and Neary T.J. The limbic system of tetrapods: a comparative analysis of cortical and amygdalar populations. Brain Behav. Evol. 46 (1995) 224-234
14. Cooke B.M., Hegstrom C.D., Keen A., and Breedlove S.M. Photoperiod and social cues influence the medial amygdala but not the bed nucleus of the stria terminalis in the Siberian hamster. Neurosci. Lett. 312 (2001) 9-12
15. Cooke B.M., Tabibnia G., and Breedlove S.M. A brain sexual dimorphism controlled by adult circulating androgens. Proc. Natl. Acad. Sci. U S A. 96 (1999) 7538-7540
16. Crews D., Robker R., and Mendonça M. Seasonal fluctuations in brain nuclei in the red-sided garter snake and their hormonal control. J. Neurosci. 13 (1993) 5356-5364
17. Crews D., Wade J., and Wilczynski W. Sexually dimorphic areas in the brain of whiptail lizards. Brain Behav. Evol. 36 (1990) 262-270
18. De Butte M., and Pappas B.A. Pinealectomy causes hippocampal CA1 and CA3 cell loss: reversal by melatonin supplementation. Neurobiol. Aging. 28 (2007) 306-313
19. Delgado-González F.J., Alonso-Fuentes A., Delgado-Fumero A., García-Verdugo J.M., González-Granero S., Trujillo-Trujillo C.M., and Damas-Hernández M.C. Seasonal differences in ventricular proliferation of adult Gallotia galloti lizards. Brain Res. 1191 (2008) 39-46
20. Dloniak S.M., and Deviche P. Effects of testosterone and photoperiodic condition on song production and vocal control region volumes in adult male dark-eyed juncos (Junco hyemalis). Horm. Behav. 39 (2001) 95-105
21. Edwards N., Kriegsfeld L., and Crews D. Neural substrates for sexual and thermoregulatory behavior in the male leopard gecko, Eublepharis macularius. Brain Res. 1029 (2004) 77-83
22. Emery D.E., and Moss R.L. Lesions confined to the ventromedial hypothalamus decrease the frequency of coital contacts in female rats. Horm. Behav. 18 (1984) 313-329
23. Farragher K., and Crews D. The role of the basal hypothalamus in the regulation of reproductive behavior in the lizard, Anolis carolinensis: lesion studies. Horm. Behav. 13 (1979) 185-206
24. Fester L., Ribeiro-Gouveia V., Prange-Kiel J., von Schassen C., Böttner M., Jarry H., and Rune G.M. Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. J. Neurochem. 97 (2006) 1136-1144
25. Fowler C.D., Liu Y., Ouimet C., and Wang Z. The effects of social environment on adult neurogenesis in the female prairie vole. J. Neurobiol. 51 (2002) 115-128
26. Friedman D.W., and Crews D. Role of the anterior hypothalamus-preoptic area in the regulation of courtship behavior in the male Canadian red-sided garter snake (Thamnophis sirtalis parietalis): lesion experiments. Behav. Neurosci. 99 (1985) 942-949
27. Godwin J., and Crews D. Hormones, brain, and behavior in reptiles. In: Pfaff D.W., Arnold A.P., Etgen A.M., Fahrbach S.E., and Rubin R.T. (Eds). Hormones, Brain and Behavior vol. 2 (2002), Academic Press, San Diego, CA 545-586
28. Gorski R.A., Gordon J.H., Shryne J.E., and Southam A.M. Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res. 148 (1978) 333-346
29. Gorski R.A., Harlan R.E., Jacobson C.D., Shryne J.E., and Southam A.M. Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat. J. Comp. Neurol. 193 (1980) 529-539
30. Gréco B., Edwards D.A., Michael R.P., and Clancy A.N. Androgen receptors and estrogen receptors are colocalized in male rat hypothalamic and limbic neurons that express Fos immunoreactivity induced by mating. Neuroendocrinology 67 (1998) 18-28
31. Greenberg N., Scott M., and Crews D. Role of the amygdala in the reproductive and aggressive behavior of the lizard, Anolis carolinensis. Physiol. Behav. 32 (1984) 147-151
32. Greenough W.T., Carter C.S., Steerman C., and Devoogd T.J. Sex differences in dendritic patterns in hamster preoptic area. Brain Research 126 (1977) 63-72
33. Hidalgo A., Barami K., Iversen K., and Goldman S.A. Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J. Neurobiol. 27 (1995) 470-487
34. Holmes M.M., Rosen G.J., Jordan C.L., de Vries G.J., Goldman B.D., and Forger N.G. Social control of brain morphology in a eusocial mammal. Proc. Natl. Acad. Sci. U S A. 104 (2007) 10548-10552
35. Huddleston G.G., Paisley J.C., and Clancy A.N. Effects of estrogen in the male rat medial amygdala: infusion of an aromatase inhibitor lowers mating and bovine serum albumin-conjugated estradiol implants do not promote mating. Neuroendocrinology 83 (2006) 106-116
36. Jaita G., Candolfi M., Zaldivar V., Zárate S., Ferrari L., Pisera D., Castro M.G., and Seilicovich A. Estrogens up-regulate the Fas/FasL apoptotic pathway in lactotropes. Endocrinology 146 (2005) 4737-4744
37. Jenssen T.A., Lovern M.B., and Congdon J.D. Field-testing the protandry-based mating system for the lizard, Anolis carolinensis: Does the model organism have the right model?. Behav. Ecol. Sociobiol. 50 (2001) 162-172
38. Jones R.E., Guillette Jr. L.J., Summers C.H., Tokarz R.R., and Crews D. The relationship among ovarian condition, steroid hormones, and estrous behavior in Anolis carolinensis. J. Exp. Zool. 227 (1983) 145-154
39. Kabelik D., Weiss S.L., and Moore M.C. Steroid hormone mediation of limbic brain plasticity and aggression in free-living tree lizards, Urosaurus ornatus. Horm. Behav. 49 (2006) 587-597
40. Kendrick A.M., Rand M.S., and Crews D. Electrolytic lesions to the ventromedial hypothalamus abolish receptivity in female whiptail lizards, Cnemidophorus uniparens. Brain Res. 680 (1995) 226-228
41. Krohmer R.W., and Crews D. Facilitation of courtship behavior in the male red-sided garter snake following lesions of the septum or nucleus sphericus. Physiol. Behav. Neurosci. 40 (1987) 759-765
42. Kim D.H., Lilliehook C., Roides B., Chen Z., Chang M., Mobashery S., and Goldman S.A. Testosterone-induced matrix metalloproteinase activation is a checkpoint for neuronal addition to the adult songbird brain. J. Neurosci. 28 (2008) 208-216
43. Kirn J., O'Loughlin B., Kasparian S., and Nottebohm F. Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. Proc. Natl. Acad. Sci. U S A. 91 (1994) 7844-7848
44. Lanuza E., Belekhova M., Martínez-Marcos A., Font C., and Martínez-García F. Identification of the reptilian basolateral amygdala: an anatomical investigation of the afferents to the posterior dorsal ventricular ridge of the lizard Podarcis hispanica. Eur. J. Neurosci. 10 (1998) 3517-3534
45. La Vaque T.J., and Rodgers C.H. Recovery of mating behavior in the female rat following VMH lesions. Physiol. Behav. 14 (1975) 59-63
46. Lovern M.B., Holmes M.M., and Wade J. The green anole (Anolis carolinensis): a reptilian model for laboratory studies of reproductive morphology and behavior. ILAR J. 45 (2004) 54-64
47. Lovern M.B., McNabb F.M., and Jenssen T.A. Developmental effects of testosterone on behavior in male and female green anoles (Anolis carolinensis). Horm. Behav. 39 (2001) 131-143
48. Lovern M.B., and Wade J. Maternal plasma and egg yolk testosterone concentrations during embryonic development in green anoles (Anolis carolinensis). Gen. Comp. Endocrinol. 124 (2001) 226-235
49. Madeira M.D., Leal S., and Paula-Barbosa M.M. Stereological evaluation and Golgi study of the sexual dimorphisms in the volume, cell numbers, and cell size in the medial preoptic nucleus of the rat. J. Neurocytol. 28 (1999) 131-148
50. Martinez-Vargas M.C., Keefer D.A., and Stumpf W.E. Estrogen localization in the brain of the lizard, Anolis carolinensis (1). J. Exp. Zool. 205 (1978) 141-147
51. Mason P., and Adkins E.K. Hormones and social behavior in the lizard, Anolis carolinensis. Horm. Behav. 7 (1976) 75-86
52. Matsumoto A., and Arai Y. Sex difference in volume of the ventromedial nucleus of the hypothalamus in the rat. Endocrinol. Jpn. 30 (1983) 277-280
53. Meisel R.L., and Sachs B.D. The physiology of male sexual behavior. In: Knobil E., and Neill J.D. (Eds). The Physiology of Reproduction. 2nd ed. vol. 2 (1994), Raven Press, New York 3-105
54. Neal J.K., and Wade J. Courtship and copulation in the adult male green anole: effects of season, hormone and female contact on reproductive behavior and morphology. Behav. Brain Res. 177 (2007) 177-185
55. Nottebohm F. Testosterone triggers growth of brain vocal control nuclei in adult female canaries. Brain Res. 189 (1980) 429-436
56. O'Bryant E.L., and Wade J. Seasonal and sexual dimorphisms in the green anole forebrain. Horm. Behav. 41 (2002) 384-395
57. Panzica G.C., Viglietti-Panzica C., Calcagni M., Anselmetti G.C., Schumacher M., and Balthazart J. Sexual differentiation and hormonal control of the sexually dimorphic preoptic medial nucleus in quail. Brain Res. 416 (1987) 59-68
58. Park J.H., Cho H., Kim H., and Kim K. Repeated brief epileptic seizures by pentylenetetrazole cause neurodegeneration and promote neurogenesis in discrete brain regions of freely moving adult rats. Neuroscience 140 (2006) 673-684
59. Pencea V., Bingaman K.D., Wiegand S.J., and Luskin M.B. Infusion of brain-derived neurotrophic factor into the lateral ventricle of the adult rat leads to new neurons in the parenchyma of the striatum, septum, thalamus, and hypothalamus. J. Neurosci. 21 (2001) 6706-6717
60. Pfaff D.W., and Sakuma Y. Facilitation of the lordosis reflex of female rats from the ventromedial nucleus of the hypothalamus. J. Physiol. 288 (1979) 189-202
61. Rasika S., Nottebohm F., and Alvarez-Buylla A. Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc. Natl. Acad. Sci. U S A. 91 (1994) 7854-7858
62. Reiner A., Perkel D.J., Bruce L.L., Butler A.B., Csillag A., Kuenzel W., Medina L., Paxinos G., Shimizu T., Striedter G., Wild M., Ball G.F., Durand S., Güntürkün O., Lee D.W., Mello C.V., Powers A., White S.A., Hough G., Kubikova L., Smulders T.V., Wada K., Dugas-Ford J., Husband S., Yamamoto K., Yu J., Siang C., and Jarvis E.D. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473 (2004) 377-414
63. Riters L.V., Eens M., Pinxten R., Duffy D.L., Balthazart J., and Ball G.F. Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm. Behav. 38 (2000) 250-261
64. Robarts D.W., and Baum M.J. Ventromedial hypothalamic nucleus lesions disrupt olfactory mate recognition and receptivity in female ferrets. Horm. Behav. 51 (2007) 104-113
65. Roselli C.E., Larkin K., Schrunk J.M., and Stormshak F. Sexual partner preference, hypothalamic morphology and aromatase in rams. Physiol. Behav. 83 (2004) 233-245
66. Rosen G., O'Bryant E., Matthews J., Zacharewski T., and Wade J. Distribution of androgen receptor mRNA expression and immunoreactivity in the brain of the green anole lizard. J. Neuroendocrinol. 14 (2002) 19-28
67. Rozendaal J.C., and Crews D. Effects of intracranial implantation of dihydrotestosterone on sexual behavior in male Cnemidophorus inornatus, a direct sexual ancestor of a parthenogenetic lizard. Horm. Behav. 23 (1989) 194-202
68. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., and Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192 (2005) 348-356
69. Smith G.T., Brenowitz E.A., and Wingfield J.C. Roles of photoperiod and testosterone in seasonal plasticity of the avian song control system. J. Neurobiol. 32 (1997) 426-442
70. Smith G.T., Brenowitz E.A., Beecher M.D., and Wingfield J.C. Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J. Neurosci. 17 15 (1997) 6001-6010
71. Takahashi L.K., and Lisk R.D. Estrogen action in anterior and ventromedial hypothalamus and the modulation of heterosexual behavior in female golden hamsters. Physiol. Behav. 34 (1985) 233-239
72. Tobet S.A., Zahniser D.J., and Baum M.J. Sexual dimorphism in the preoptic/anterior hypothalamic area of ferrets: effects of adult exposure to sex steroids. Brain Res. 364 (1986) 249-257
73. Tokarz R.R., and Crews D. Induction of sexual receptivity in the female lizard, Anolis carolinensis: effects of estrogen and the antiestrogen CL-628. Horm. Behav. 14 (1980) 33-45
74. Tramontin A.D., and Brenowitz E.A. Seasonal plasticity in the adult brain. Trends Neurosci. 23 (2000) 251-258
75. Tunç A.T., Turgut M., Aslan H., Sahin B., Yurtseven M.E., and Kaplan S. Neonatal pinealectomy induces Purkinje cell loss in the cerebellum of the chick: a stereological study. Brain Res. 1067 (2005) 95-102
76. Vagell M.E., and McGinnis M.Y. The role of aromatization in the restoration of male rat reproductive behavior. J. Neuroendocrinol. 9 (1997) 415-421
77. Wade J. Androgen metabolism in the brain of the green anole lizard (Anolis carolinensis). Gen. Comp. Endocrinol. 106 (1997) 127-137
78. Wade J., and Crews D. The relationship between reproductive state and "sexually" dimorphic brain areas in sexually reproducing and parthenogenetic whiptail lizards. J. Comp. Neurol. 309 (1991) 507-514
79. Wade J., and Crews D. Sexual dimorphisms in the soma size of neurons in the brain of whiptail lizards (Cnemidophorus species). Brain Res. 594 (1992) 311-314
80. Wade J., Huang J.M., and Crews D. Hormonal control of sex differences in the brain, behavior and accessory sex structures of whiptail lizards (Cnemidophorus species). J. Neuroendocrinol. 5 (1993) 81-92
81. Wheeler J.M., and Crews D. The role of the anterior hypothalamus-preoptic area in the regulation of male reproductive behavior in the lizard, Anolis carolinensis: lesion studies. Horm. Behav. 11 (1978) 42-60
82. Wiechmann A.F., and Wirsig-Wiechmann C.R. Melatonin receptor distribution in the brain and retina of a lizard, Anolis carolinensis. Brain Behav. Evol. 43 (1994) 26-33
83. Winkler S.M., and Wade J. Aromatase activity and regulation of sexual behaviors in the green anole lizard. Physiol. Behav. 64 (1998) 723-731
84. Wu J., Whittier J.M., and Crews D. Role of progesterone in the control of female sexual receptivity in Anolis carolinensis. Gen. Comp. Endocrinol. 58 (1985) 402-406