The expression of brain sexual dimorphism in artificial selection of rat strains

Brain Research

Volumn 1052, Issue 2, 2005, Pages 130-138

  Garcia Falgueras, Alicia ^a   Pinos, Helena ^a   Collado, Paloma ^a   Pasaro, Eduardo ^b   Fernandez, Rosa ^b   Segovia, Santiago ^a   Guillamon, Antonio ^a  

^a UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

^b UNIVERSITY OF A CORUÑA   (Spain)

Author keywords

Artificial selection; Bed nucleus of the stria terminalis; Brain sex difference; Locus coeruleus; Long Evans rat; Sex difference; Strain difference; Vomeronasal system; Wistar rat

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; ARTIFICIAL SELECTION; BRAIN; CELL NUCLEUS; CENTRAL NERVOUS SYSTEM; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; LABORATORY; LOCUS CERULEUS; MALE; MEASUREMENT; MORPHOLOGY; NERVE CELL; NONHUMAN; PHYLOGENY; PIGMENTATION; PRIORITY JOURNAL; RAT; RAT STRAIN; SEX DIFFERENCE; SEX RATIO; SEXUAL BEHAVIOR; STRIA TERMINALIS; STRUCTURE ANALYSIS;

ANIMALS; CELL COUNT; FEMALE; LOCUS COERULEUS; MALE; RATS; RATS, LONG-EVANS; RATS, WISTAR; SELECTION (GENETICS); SEPTAL NUCLEI; SEX CHARACTERISTICS; SEX FACTORS; SPECIES SPECIFICITY;

EID: 23644462083     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2005.05.066     Document Type: Article

References (85)

1. P. Absil, M. Papello, C. Viglietti-Panzica, J. Balthazart, and G. Panzica The medial preoptic nucleus receives vasotocinergic inputs in male quail: a tract-tracing and immunocytochemical study J. Chem. Neuroanat. 24 2002 27 39
2. S. Alhenius, J. Engel, H. Eriksson, K. Modigh, and P. Sodersten Involvement of monoamines in the mediation of lordosis behavior M. Sandler G.L. Gessa Sexual Behavior: Pharmacology and Biochemistry 1975 Raven Press New York 137 145
3. L.S. Allen, and R.A. Gorski Sex difference in the bed nucleus of the stria terminalis of the human brain J. Comp. Neurol. 302 1990 697 706
4. D. Babstock, C.W. Malsbury, and C.W. Harley The dorsal locus coeruleus is larger in male than in female Sprague-Dawley rats Neurosci. Lett. 224 1997 157 160
5. J. Balthazart Correlation between the sexually dimorphic aromatase of the preoptic area and sexual behavior in quail: effects of neonatal manipulations of the hormonal milieu Arch. Int. Physiol. Biochim. 97 1989 465 481
6. J.F. Bellringer, H.P. Pratt, and E.B. Keverne Involvement of the vomeronasal organ and prolactin in pheromonal induction of delayed implantation in mice Reproduction 59 1980 223 228
7. C.H. Busch, H. Braak, J. Bohl, and T.G. Ohm The human nucleus coeruleus in aging-A sterological analysis of females and males Abstr.-Soc. Neurosci. 21 1995 1565
8. W. Byne The medial preoptic and anterior hypothalamic regions of the rhesus monkey: cytoarchitectonic comparison with the human and evidence for sexual dimorphism Brain Res. 18 1998 346 350
9. F. Claro, S. Segovia, A. Guilamon, and A. Del Abril Lesions in the medial posterior region of the BST impair sexual behavior in sexually experienced and inexperienced male rats Brain Res. Bull. 36 1995 1 10
10. W.C.J. Chung, D.F. Swaab, and G.J. De Vries Apoptosis during sexual differentiation of the bed nucleus of the stria terminalis J. Neurobiol. 43 2000 234 243
11. W.C.J. Chung, G.J. De Vries, and D.F. Swaab Sexual differentiation of the bed nucleus of the stria terminalis in humans may extend into adulthood J. Neurosci. 22 2002 1027 1033
12. A. Dahlström, and K. Fuxe Evidence for the existence of monoamine-containing neurons in the central nervous system: I. Demonstration of monoamines in the cell bodies of brain stem neurons Acta Physiol. Scand. 62 1964 1 55
13. Ch. Darwin. On the origin of species by means of natural selection. Londres, John Murray, 1859. Reprinting Harvard University Press, 1964.
14. The descendent of man, and selection in relation to sex. Londres, John Murray, 1871. Reprinting Princeton University Press, 1981.
15. M.R. De Blas, M. Rodriguez-Zafra, C. Perez-Laso, P. Collado, A. Del Abril, M.C.R. Del Cerro, S. Segovia, and A. Guillamon Feminization of the rat locus coeruleus: the role of estradiol Conf. Reprod. Behav. 27 1995 112 (Abstract)
16. J.S. De Olmos, G.F. Alheid, and C.A. Beltramino Amygdala G. Paxinos The Rat Nervous System vol. I 1985 Academic Press Sydney 223 234
17. A. Del Abril, S. Segovia, and A. Guillamon The bed nucleus of the stria terminalis in the rat: regional sex differences controlled by gonadal steroid early after birth Dev. Brain Res. 32 1987 295 300
18. M.C. Del Cerro, M.A. Izquierdo, P. Collado, S. Segovia, and A. Guillamon Bilateral lesions of the bed nucleus of the accessory olfactory tract facilitate maternal behavior in virgin female rats Physiol. Behav. 50 1991 67 71
19. M.C. Diamond, R.E. Johnson, and J.A. Ehlert Comparison of cortical thickness in male and female rats-normal and gonadectomized, young and adult Behav Neural Biol. 26 1979 485 491
20. M.C. Diamond, G.A. Dowling, and R.E. Johnson Morphologic cerebral cortical asymmetry in male and female rats Exp. Neurol. 71 1981 261 268
21. M.C. Diamond Hormonal effects on the development or cerebral lateralization Psychoneuroendocrinology 16 1991 121 129
22. LE. Eiden, T. Hokfelt, M.J. Brownstein, and M. Palkovits Vasoactive intestinal polypeptide afferents to the bed nucleus of the stria terminalis in the rat: an immunohistochemical and biochemical study Neuroscience 15 1985 999 1013
23. D.E. Emery, and B.D. Sachs Copulatory behavior in male rats with lesions in the bed nucleus of the stria terminalis Physiol. Behav. 17 1976 803 806
24. A. Fleming, F. Vaccarino, L. Tambosso, and P. Chee Vomeronasal and olfactory system modulation of maternal behavior in the rat Science 203 1979 372 374
25. R.A. Gorski, J.H. Gordon, J.E. Shryne, and A.M. Southam Evidence for a morphological sex difference within the medial preoptic area of the rat brain Brain Res. 148 1978 333 346
26. R.A. Gorski, R.E. Harlan, C.D. Jacobson, J.E. Shryne, and A.M. Southam Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat J. Comp. Neurol. 193 1980 529 539
27. W.T. Greenough, C.S. Carter, C. Steerman, and T.J. DeVoogd Sex differences in dentritic patterns in hamster preoptic area Brain Res. 126 1977 63 72
28. A. Guillamon, and S. Segovia Sexual dimorphismin the CNS and the role of steroids T.W. Stone Neurotransmitters and Neuromodulators Neuroactive Steroids 1996 CRC Press Florida 127 152
29. A. Guillamon, M.R. De Blas, and S. Segovia Effects of sex steroids on the development of the locus coeruleus in the rat Dev. Brain Res. 40 1988 306 310
30. A. Guillamon, S. Segovia, and A. Del Abril Early effects of gonadal steroids on the neuron number in the medial posterior region and the lateral division of the bed nucleus of the stria terminalis in the rat Dev. Brain Res. 44 1988 281 290
31. H.J.G. Gundersen, P. Bagger, T.F. Bendtsen, S.M. Evans, L. Korbo, N. Marcussen, A. Moller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sorensen, A. Vesterby, and M.J. West The new stereologicals tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis APMIS 96 1988 857 881
32. H.J.G. Gundersen, T.F. Bendtsen, L. Korbo, N. Marcussen, A. Moller, K. Nielsen, J.R. Nyengaard, B. Pakkenberg, F.B. Sorensen, A. Vesterby, and M.J. West Some new, simple and efficient stereological methods and their use in pathological research and diagnosis APMIS 96 1988 379 394
33. E.L. Gustafson, and P. Greengard Localization of DARPP-32 immunoreactive neurons in the bed nucleus of the stria terminalis and central nucleus of the amygdala: co-distribution with axons containing tyrosine hydroxylase, vasoactive intestinal polypeptide, and calcitonin gene-related peptide Exp. Brain Res. 79 1990 447 458
34. M. Halpern The organization and function of the vomeronasal system Annu. Rev. Neurosci 10 1987 325 362
35. M. Halpern, and A. Martinez-Marcos Structure and function of the vomeronasal system: an update Prog. Neurobiol. 70 2003 245 318
36. T.M. Han, and G.J. De Vries Neurogenesis of galanin cells in the bed nucleus of the stria terminalis and centromedial amygdala in rats: a model for sexual differentiation of neuronal phenotype J. Neurobiol. 38 1999 491 498
37. A.E. Herbison Sexually dimorphic expression of androgen receptor immunoreactivity by somatostatin neurones in rat hypothalamic periventricular nucleus and bed nucleus of the stria terminalis J. Neuroendocrinol. 7 1995 543 553
38. M. Hines, F.C. Davis, A. Coquelin, R.W. Goy, and R.A. Gorski Sexually dimorphic regions in the medial preoptic area and the bed nucleus of the stria terminalis of the guinea pig brain: a description and an investigation of their relationship to gonadal steroids in adulthood J. Neurosci. 5 1985 40 47
39. M.A. Hofman, and D.F. Swaab The sexually dimorphic nucleus of the preoptic area in the human brain: a comparative morphometric study J. Anat. 164 1989 55 72
40. M.A. Izquierdo, P. Collado, S. Segovia, A. Guillamon, and M.C. del Cerro Maternal behavior induced in male rats by bilateral lesions of the bed nucleus of the accessory olfactory tract Physiol. Behav. 52 1992 707 712
41. C.D. Jacobson, and R.A. Gorski Neurogenesis of the sexually dimorphic nucleus of the preoptic area in the rat J. Comp. Neurol. 196 1981 519 529
42. M.A. Johns The role of the vomeronasal organ in behavioral control of reproduction Ann. N. Y. Acad. Sci. 474 1986 148 157
43. G. Ju, and Z. Han Coexistence of corticotropin releasing factor and neurotensin within oval nucleus neurons in the bed nuclei of the stria terminalis in the rat Neurosci. Lett. 99 1989 246 250
44. A. Jurkevich, S.W. Barth, N. Aste, G. Panzica, and R. Grossmann Intracerebral sex differences in the vasotocin system in birds: possible implication in behavioral and autonomic functions Horm. Behav. 30 1996 673 681
45. A. Jurkevich, S.W. Barth, W.J. Kuenzel, A. Kohler, and R. Grossmann Development of sexually dimorphic vasotocinergic system in the bed nucleus of stria terminalis in chickens J. Comp. Neurol. 408 1999 46 60
46. C. Kelche, and C. Aron Olfactory cues and accessory olfactory bulb lesion: effects on sexual behavior in the cyclic female rat Physiol. Behav. 33 1984 45 48
47. F.P.M. Kruijver, J.-N. Zhou, C.W. Pool, M.A. Hofman, L.J.G. Gooren, and D.F. Swaab Male-to-female transsexuals have female neuron numbers in a limbic nucleus J. Clin. Endocrinol. Metab. 85 2000 2034 2041
48. M.N. Lehman, S.S. Winans, and JB. Powers Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior Science 210 1980 557 560
49. C.A. Lisciotto, and J.I. Morrell Sex differences in the distribution and projections of testosterone target neurons in the medial preoptic area and the bed nucleus of the stria terminalis of rats Horm. Behav. 28 1994 492 502
50. J.M. Luque, M.R. De Blas, S. Segovia, and A. Guillamon Sexual dimorphism of the dopamine-β-hydroxylase-immunoreactive neurons in the rat locus coeruleus Dev. Brain Res. 67 1992 211 215
51. M. Meredith Sensory processing in the main and accessory olfactory systems: comparisons and contrasts J. Steroid. Biochem. Mol. Biol. 39 1991 601 614
52. R. Michael, and L.M. Cruz-Orive Application of the Cavalieri principle, and vertical sections method to lung; estimation of volume and pleural surface area J. Microsc. 150 1988 117 136
53. J.C. Mitchell, X.F. Li, L. Breen, J.-C. Thalabard, and K.T. O'Byrne The role of the locus coeruleus in corticotropin-releasing hormone and stress-induced suppression of pulsatile luteinizing hormone secretion in the female rat Endocrinology 146 2005 (Jan.) 323 331
54. R.J. O'Connell, and M. Meredith Effects of volatile and nonvolatile chemical signals on male sex behaviors mediated by the main and accessory olfactory systems Behav. Neurosci. 98 1984 1083 1093
55. G. Panzica, C. Viglietti-Panzica, and J. Balthazart Sexual dimorphism in the neuronal circuits of the quail preoptic and limbic regions Microsc. Res. Tech. 54 2001 364 374
56. G.C. Panzica, J. Bakthazart, M. Pessatti, and C. Viglietti-Panzica The parvocellular vasotocin system of Japanese quail: a developmental and adult model for the study of influences of gonadal hormones on sexually differentiated and behaviorally relevant neural circuits Environ. Health Perspect. 110 2002 423 428
57. D. Pass, and G. Freeth The rat Anzccart News 6 1993 1 4
58. G. Paxinos, C. Watson, The Rat Brain in Stereotaxic Coordinates, Fourth Edition. New York: Academic Press, Spiral Bound, 1998.
59. H. Pinos, P. Collado, M. Rodríguez-Zafra, C. Rodríguez, S. Segovia, and A. Guillamon The development of sex differences in the locus coeruleus of the rat Brain Res. Bull. 56 2001 73 78
60. B. Planas, P.E. Kolb, M.A. Raskind, and M.A. Miller Activation of galanin pathways across puberty in the male rat: galanin gene expression in the bed nucleus of the stria terminalis and medial amygdala Neuroscience 63 1994 851 858
61. B. Planas, P.E. Kolb, M.A. Raskind, and M.A. Miller Sex difference in coexpression by galanin neurons accounts for sexual dimorphism of vasopressin in the bed nucleus of the stria terminalis Endocrinology 136 1995 727 733
62. B. Powers, and E.S. Valenstein Sexual receptivity: facilitation by medial preoptic lesions in female rats Science 175 1972 1003 1005
63. Ch.E. Roselli, K. Larkin, J.A. Resko, J.N. Stellflug, and F. Stormshak The volume of a sexually dimorphic nucleus in the ovine medial preoptic area/anterior hypothalamus varies with sexual partner preference Endocrinology 145 2004 478 483
64. T.R. Saito, and H. Moltz Copulatory behavior of sexually naive and sexually experienced male rats following removal of the vomeronasal organ Physiol. Behav. 37 1986 507 510
65. T.R. Saito, and H. Moltz Sexual behavior in the female rat following removal of the vomeronasal organ Physiol. Behav. 38 1986 81 87
66. S. Segovia, and A. Guillamon Sexual dimorphism in the vomeronasal pathway and sex differences in reproductive behaviors Brain Res. Brain Res. Rev. 18 1993 51 74
67. S. Segovia, and A. Guillamon Searching for sex differences in the vomeronasal pathway Horm. Behav. 30 1996 618 626
68. S. Segovia, A. Guillamon, M.C. del Cerro, E. Ortega, C. Perez-Laso, M. Rodriguez-Zafra, and C. Beyer The development of brain sex differences: a multisignaling process Behav. Brain Res. 105 1999 69 80
69. L.E. Shapiro, C.M. Leonard, C.E. Sessions, D.A. Dewsbury, and T.R. Insel Comparative neuroanatomy of the sexually dimorphic hypothalamus in monogamous and polygamous voles Brain Res. 15 1991 232 240
70. M.T. Shipley, M. Ennis, and A.C. Puche Olfatory system G. Paxinos The Rat Nervous System 3rd ed. 2004 Elsevier Academic Press 923 964
71. R.B. Simerly, and L.W. Swanson The organization of neural inputs to the medial preoptic nucleus of the rat J. Comp. Neurol. 245 1986 312 342
72. T. Steimer, and J.B. Hutchison Is androgen-dependent aromatase activity sexually differentiated in the rat and dove preoptic area? J. Neurobiol. 21 1990 787 795
73. D.C. Sterio The unbiased estimation of number and sizes of arbitrary particles using the disector J. Microsc. 134 1984 127 136
74. D.F. Swaab, and E. Fliers A sexually dimorphic nucleus in the human brain Science 228 1985 1112 1115
75. D.F. Swaab, and M.A. Hofman Sexual differentiation of the human hypothalamus in relation to gender and sexual orientation Trends Neurosci. 18 1995 264 270
76. D.F. Swaab, W.C. Chung, F.P. Kruijver, M.A. Hofman, and T.A. Ishunina Structural and functional sex differences in the human hypothalamus Horm. Behav. 40 2001 93 98
77. L.W. Swanson, and B.K. Hartman The central adrenergic system. An inmunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta hydroxylase as a marker J. Comp. Neurol. 163 1975 467 506
78. F.W. van Leeuwen, A.R. Caffe, and G.J. De Vries Vasopressin cells in the bed nucleus of the stria terminalis of the rat: sex differences and the influence of androgens Brain Res. 325 1985 391 394
79. C. Viglietti-Panzica, G.C. Panzica, M.G. Fiori, M. Calcagni, G.C. Anselmetti, and J. Balthazart A sexually dimorphic nucleus in the quail preoptic area Neurosci Lett. 64 1986 129 134
80. T.A. Voorhuis, J.Z. Kiss, E.R. de Kloet, and D. de Wied Testosterone sensitive vasotocin-immunoreactive cells and fibers in the canary brain Brain Res. 442 1988 139 146
81. R.I. Wood, and S.W. Newman Androgen receptor immunoreactivity in the male and female Syrian hamster brain J. Neurobiol. 39 1999 359 370
82. PL. Woodhams, GW. Roberts, JM. Polak, and TJ. Crow Distribution of neuropeptides in the limbic system of the rat: the bed nucleus of the stria terminalis, septum and preoptic area Neuroscience 8 1983 677 703
83. C.J. Wysocki Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction Neurosci. Biobehav. Rev. 3 1979 301 341
84. J.N. Zhou, M.A. Hofman, L.J. Gooren, and D.F. Swaab A sex difference in the human brain and its relation to transsexuality Nature 378 1995 68 70
85. L.M. Zucker Two way selection for body size in rats, with observation on simultaneous changes in coat color pattern and hood size Genetics 45 1960 467 483