Sexual dimorphism in the vomeronasal pathway and sex differences in reproductive behaviors

Akwa, 1991, Neurosteroids:biosynthesis, metabolism and function of pregnenolone and dehydroepiandrosterone in the brain, J. Steroid Biochem. Mol. Biol., 40, 71, 10.1016/0960-0760(91)90169-6 Alberts, 1990, Functional organization of dyadic and triadic parent-offspring systems, 416 Allen, 1990, Sex difference in the bed nucleus of the stria terminalis of the human brain, J. Comp. Neural., 302, 697, 10.1002/cne.903020402 Allison, 1953, The morphology of the olfactory system in vertebrates, Biol. Rev., 28, 195, 10.1111/j.1469-185X.1953.tb01376.x Anderson, 1986, Relationships between sexual activity, plasma testosterone and the volume of the sexually dimorphic nucleus of the preoptic area in prenatally stressed and non-stressed rats, Brain Res., 370, 1, 10.1016/0006-8993(86)91098-X Anderson, 1985, Effects of prenatal stress on differentiation of the sexually dimorphic nucleus of thepreoptic area (SDN-POA) of the rat brain, Brain Res., 332, 113, 10.1016/0006-8993(85)90394-4 Arendash, 1982, Enhancement of sexual behavior in female rats by neonatal transplantation of brain tissue from males, Science, 217, 1276, 10.1126/science.7112132 Arendash, 1983, Effects of discrete lesions of the sexually dimorphic nucleus of the preoptic area or other medial preoptic regions on the sexual behavior of male rats, Brain Res. Bull., 10, 147, 10.1016/0361-9230(83)90086-2 Arnold, 1985, Organizational and activational effects of sex steroids on brain and behavior: a reanalysis, Hormones Behav., 19, 469, 10.1016/0018-506X(85)90042-X Arnold, 1984, Gonadal steroid induction of structural sex differences in the central nervous system, Annu. Reu. Neurosci., 7, 413, 10.1146/annurev.ne.07.030184.002213 Baulieu, 1990, Neurosteroids: a new brain function?, J. Steroid Biochem. Mol. Biol., 37, 395, 10.1016/0960-0760(90)90490-C Bayer, 1979, The development of the septal region in the rat. I. Neurogenesis examined with [3H]thymidine autoradiography, J. Comp. Neurol., 183, 89, 10.1002/cne.901830108 Bayer, 1980, Quantitative [3]HThymidine-radiographic analyses of neurogenesis in the rat amygdala, J. Comp. Neurol., 194, 845, 10.1002/cne.901940409 Bayer, 1983, 3H]Thymidine-radiographic studies of neurogenesis in the rat olfactory bulb, Exp. Brain Res., 50, 329, 10.1007/BF00239197 Bellringer, 1980, Involvement of the vomeronasal organ and prolactin in pheromonal induction of delayed implantation in mice, J.Reprod. Fertil., 59, 223, 10.1530/jrf.0.0590223 Beltramino, 1979, Effect of electrochemical stimulation of the olfactory bulbs on the release of gonadotropin hormones in rats, Neuroendocrinology, 28, 320, 10.1159/000122879 Beltramino, 1980, Dual action of electrochemical stimulation of the bed nucleus of the stria terminalis on the release of LH, Neuroendocrinology, 30, 238, 10.1159/000123007 Beltramino, 1985, Ventral premammillary nuclei mediate pheromonal-induced LH release stimuli in the rat, Neuroendocrinology, 41, 119, 10.1159/000124164 Berk, 1981, Afferent projections to the preoptic area and hypothalamic regions in the rat brain, Neuroscience, 6, 1601, 10.1016/0306-4522(81)90227-X Beyer, 1987, Sex steroids and afferent input: their roles in brain sexual differentiation, Annu. Rev. Physiol., 49, 349, 10.1146/annurev.ph.49.030187.002025 Bleier, 1982, Citoarchitectonic sexual dimorphisms of the medial preoptic and anterior hypothalamic areas in guinea pig, rat, hamster and mouse, , J. Comp. Neurol., 212, 118, 10.1002/cne.902120203 Bloch, 1988, Cytoarchitectonic analysis of the SDN-POA of the intact and gonadectomized rat, J. Comp. Neurol., 275, 604, 10.1002/cne.902750408 Bloch, 1988, Estrogen/progesterone treatment in adulthood affects the size of several components of the medial preoptic area in the male rat,, J. Comp. Neurol., 275, 613, 10.1002/cne.902750409 Brenowitz, 1985, Neural correlates of female song in tropical duelling birds, Brain Res., 334, 104, 10.1016/0006-8993(85)91163-1 Broadwell, 1975, Olfactory relationships of the telencephalon and diencephalon in the rabbit.I.An autoradiographic study of the efferent connections of the main and accessory olfactory bulbs, J. Comp. Neurol., 163, 329, 10.1002/cne.901630306 Byne, 1987, Medial preoptic sexual dimorphisms in the guinea pig. I. An investigation on their hormonal dependence, J. Neurosci., 7, 2688, 10.1523/JNEUROSCI.07-09-02688.1987 Caminero, 1989, Efecto de los esteroides gonadales sobre lascelulas mitrales del bulbo olfatorio accesorio de la rata Caminero, 1990, The accessory olfactory bulb of the rat: a Golgi study, Eur. J. Neurosci. Suppl. No. 3, 136 Caminero, 1991, Sexual dimorphism in accessory olfactory bulb mitral cells: a quantitative Golgi study, Neuroscience, 45, 663, 10.1016/0306-4522(91)90279-W Cedarbaum, 1978, Afferent projections to the rat locus coeruleus as determined by a retrograde tracing, J. Comp. Neurol., 178, 1, 10.1002/cne.901780102 Chateau, 1987, Effects of ventromedial nucleus lesions on the display of lordosis behavior in the male rat. Interactions with facilitatory effects of male urine, Physiol. Behav., 39, 341, 10.1016/0031-9384(87)90232-0 Chozick, 1986, The behavioral effects of lesions of the amygdala: a review, Int. J. Neurosci., 29, 205, 10.3109/00207458608986152 Collado, 1990, Efecto de los esteroides gonadales en la diferenciación del nucleo del tracto olfatorio accesorio en la rata Collado, 1990, Sexual dimorphism in the bed nucleus of the accessory olfactory tract in the rat, Dev. Brain Res., 56, 263, 10.1016/0165-3806(90)90091-C Collado, P, Segovia, S., Calés, J.M., Pérez-Laso, C., RodríguezZafra, M., Guillamón, A. and Valencia, A., Female's DHT controls sex differences in the rat bed nucleus of the accessory olfactory tract, Neuroreport, in press. Collado, 1992 Commins, 1984, Adult testosterone levels influence the morphology of a sexually dimorphic area in the mongolian gerbil brain, J. Comp. Neurol., 244, 132, 10.1002/cne.902240112 Commins, 1984, Lesions of the sexually dimorphic area disrupt mating and marking in male gerbils, Brain Res. Bull., 13, 193, 10.1016/0361-9230(84)90020-0 Commins, 1985, Autoradiographic localization of estrogen and androgen receptors in the sexually dimorphic area and other regions of the gerbil brain, J. Comp. Neurol., 231, 473, 10.1002/cne.902310406 Conrad, 1976, Efferents from medial basal forebrain and hypothalamus in the rat. I. An autoradiographic study of the medial preoptic area, J. Comp. Neurol., 169, 185, 10.1002/cne.901690205 Conrad, 1976, Efferents from medial basal forebrain and hypothalamus in the rat. II. An autoradiographic study of the anterior hypothalamus, J. Comp. Neurol., 169, 221, 10.1002/cne.901690206 Cottingham, 1986, Interconnectedness of steroid hormone-binding neurons: existence and implications, 223 Cowan, 1965, The connexions of the amygdala, J. Neurol. Neurosurg. Psychiat., 28, 137, 10.1136/jnnp.28.2.137 Davis, 1977, Studies on the action of estradiol in the regulation of sexual behavior in rats. Masculine and feminine behavior in the male Davis, 1978, Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the hamster, Brain Res. Bull., 3, 59, 10.1016/0361-9230(78)90062-X De Blas, 1988, Efecto de los esteroides gonadales en la diferen-ciación del locus coeruleus de la rata De Blas, 1990, Effects of postpuberal gonadectomy on cell population of the locus coeruleus in the rat, Med. Sci. Res., 18, 355 De Jonge, 1989, Lesions of the SDN-POA inhibit sexual behavior of male Wistar rats, Brain Res. Bull., 23, 483, 10.1016/0361-9230(89)90194-9 De Olmos, 1972, The amygdaloid projection field in the rat as studied with the cupric-silver method, 145 De Olmos, 1985, Amygdala, Vol. I, 223 De Olmos, 1978, The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study, J. Comp. Neurol., 181, 213, 10.1002/cne.901810202 De Olmos, 1972, The projection field of the stria terminalis in the rat brain. An experimental study, J. Comp. Neurol., 146, 303, 10.1002/cne.901460303 De Vries, 1990, Sex differences in neurotransmitter systems, J. Neuroendocrinol., 2, 1, 10.1111/j.1365-2826.1990.tb00385.x 1984, 61 Del Abril, 1988, Efecto de los esteroides gonadales en el desarrollo y deferenciación del nucleo de la estria terminal en la rata Del Abril, 1987, El nucleo de la estria terminal de la rata: diferencias de sexo en la población neuronal de la region medial anterior, Trabajos Instituto Cajal, LXXVI, 230 Del Abril, 1987, The bed nucleus of the stria terminalis in the rat: regional sex differences con-trolled by gonadal steroids early after birth, Dev. Brain Res., 32, 295, 10.1016/0165-3806(87)90110-6 Del Abril, 1990, Sexual dimorphism in the parastrial nucleus of the rat preoptic area, Dev. Brain Res., 52, 11, 10.1016/0165-3806(90)90216-L Del Cerro, 1991, Bilateral lesions of the bed nucleus of the accessory olfactory tract facilitate maternal behavior in virgin female rats, Physiol. Behav., 50, 67, 10.1016/0031-9384(91)90499-E Devor, 1976, Fiber trajectories of olfactory bulb efferents in the hamster, J. Comp. Neurol., 166, 31, 10.1002/cne.901660104 Döhler, 1982, Differentiation of the sexually dimorphic nucleus in the preoptic area of the rat brain is determined by the perinatal hormone environment, Neurosci. Lett., 33, 295, 10.1016/0304-3940(82)90388-3 Döhler, 1986, Pre-and postnatal influence of an estrogen antagonist and an androgen antagonist on differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats, Neuroendocrinology, 42, 443, 10.1159/000124484 Döhler, 1984, Participation of estrogens in female sexual differentiation of the brain: neuroanatomical, neuroen-docrine and behavioral evidence, Prog. Brain Res., 61, 99, 10.1016/S0079-6123(08)64430-1 Döhler, 1982, Pre- and postnatal influence of diethystilbe-strol on differentiation of sexually dimorphic nucleus in the preoptic area of the female rat brain, Neuroendocrinol. Lett., 4, 361 Dörner, 1976 Dörner, 1968, Structural changes in the preoptic nterior hypothalamic area of the male rat, following neonatal castration and androgen substitution, Neuroendocrinology, 3, 136, 10.1159/000121703 Dörner, 1969, Structural changes in the hypothala-mic ventromedial nucleus of the male rat, following neonatal castration and androgen treatment, Neuroendocrinology, 4, 278, 10.1159/000121758 Emery, 1976, Copulatory behavior in male rats with lesions in the bed nucleus of the stria terminalis, Physiol. Behav., 17, 803, 10.1016/0031-9384(76)90044-5 Fleischer, 1981, Olfactory bulbectomy and gender differences in maternal behaviors of rats, Physiol. Behav., 26, 957, 10.1016/0031-9384(81)90191-8 Fleming, 1979, Vomeronasal and olfactory system modulation of maternal behavior in rat, Science, 203, 372, 10.1126/science.760196 Fleming, 1980, Amygdaloid inhibition of maternal behavior in the nulliparus female rat, Physiol. Behav., 25, 731, 10.1016/0031-9384(80)90377-7 Ginton, 1977, Long-range effects of MPOA lesion on mating behavior in the male rat, Brain Res., 120, 158, 10.1016/0006-8993(77)90507-8 Goldschmidt, 1984, Mast cells in the rat thalamus: nuclear localization, sex difference and left-right asymmetry, Brain Res., 323, 209, 10.1016/0006-8993(84)90291-9 Gorski, 1981, Sexual dimorphism in the preoptic area,Reproduction and Development, Adr. Physiol. Sci., 15, 121 Gorski, 1978, Evidence for a morphological sex difference within the medial preoptic area of the rat brain, Brain Res., 148, 333, 10.1016/0006-8993(78)90723-0 Gorski, 1980, Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat, J. Comp. Neurol., 193, 529, 10.1002/cne.901930214 Goy, 1980 Gubernick, 1990, A maternal chemosignal maintains paternal behaviour in the biparental California mouse, Peromyscus californieus, Animal Behav., 39, 936, 10.1016/S0003-3472(05)80958-3 Gubernick, 1987, The biparental care system of the California mouse, Peromyscus californicus, J. Comp. Psychol., 101, 169, 10.1037/0735-7036.101.2.169 Gubernick, 1989, Postpartum maintenance of paternal behaviour in the biparental California mouse, Peromyscus californicus, Animal Behav., 37, 656, 10.1016/0003-3472(89)90044-4 Guillamón, 1988, Effects of sex steroids on the development of the locus coeruleus in the rat, Dev. Brain Res., 40, 306, 10.1016/0165-3806(88)90143-5 Guillamón, 1988, Early effects of gonadal steroids on the neuron number in the medial posterior and the lateral divisions of the bed nucleus of the stria terminalis in the rat, Dev. Brain Res., 44, 281, 10.1016/0165-3806(88)90226-X Gurdjian, 1927, The diencephalon of the albino rat. Studies on the brain of the rat, J. Comp. Neurol., 43, 1, 10.1002/cne.900430102 Halpern, 1987, The organization and function of the vomeronasal system, Annu. Rev. Neurosci., 10, 325, 10.1146/annurev.ne.10.030187.001545 Hammer, 1984, The sexually dimorphic region of the preoptic area in rats contains denser opiate receptor binding sites in females, Brain Res., 308, 172, 10.1016/0006-8993(84)90932-6 Heimer, 1972, The olfactory connections of the diencephalon in the rat, Brain Behav. Evol., 6, 484, 10.1159/000123728 Heimer, 1966, Impairment of mating behavior in male rats following lesions in the preoptic-anterior hypothalamic continuum, Brain Res., 3, 248, 10.1016/0006-8993(67)90076-5 Hennessey, 1986, Preoptic lesions increase the display of lordosis by male rats, Brain Res., 370, 21, 10.1016/0006-8993(86)91100-5 Heritage, 1980, Brainstem catecholamine neurons are target site for sex steroid hor mones, Science, 207, 1377, 10.1126/science.7355296 Heritage, 1981, [3H]-Di-hydrotestosterone in catecholamine neurons of the rat brain stem: combined localization by autoradiography and formaldehyde-induced fluorescence, J. Comp. Neurol., 200, 289, 10.1002/cne.902000208 Herrick, 1957, Singing female canaries, Science, 125, 1299, 10.1126/science.125.3261.1299 Hines, 1985, 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, 40, 10.1523/JNEUROSCI.05-01-00040.1985 Hofman, 1989, The sexually dimorphic nucleus of the preoptic area in the human brain: a comparative morpho metric study, J. Anat., 164, 55 Holstege, 1985, Projections of the bed nucleus of the stria terminalis to the mesencephalon, pons and medulla oblongata in the cat, Exp. Brain Res., 58, 379, 10.1007/BF00235319 Ingersoll, 1981, Role of the vomeronasal organ in murini priming and signalling chemocommunication system, Dissertation, Abstr., 41B, 3215 Izquierdo, M.A.P., Del Cerro, M.C.R., Collado ,P., Segovia, S., and Guillamón, A., Maternal behavior induced in male rats by bilateral lesions of the bed nucleus of the accessory olfactory tract, Physiol. Behav., in press. Jacobson, 1981, The influence of gonadectomy androgen exposure or a gonadalgraft in the neonatal rat on the volume of the sexually dimorphic nucleus of the preoptic area, J. Neurosci., 1, 1142, 10.1523/JNEUROSCI.01-10-01142.1981 Jacobson, 1980, Ontogeny of the sexually dimorphic nucleus of the preopticn area, J. Comp. Neurol., 193, 541, 10.1002/cne.901930215 Johns, 1980, The role of the vomeronasal system in mammalian reproductive physiology, 341 Johns, 1978, Urine-induced reflex ovulation in anovulatory rats may be a vomeronasal effect, Nature, 272, 446, 10.1038/272446a0 Johnston, 1923, Further contributions to the study of evolution of the forebrain, J. Comp. Neurol., 35, 337, 10.1002/cne.900350502 Johnston, 1983, Chemical signals and reproductive behavior, 95 Johnston, 1985, Olfactory and vomeronasal mechanisms of communication, 322 Jones, 1977, Ascending projections of the locus coeruleus in the rat. II. Autoradiographic study, Brain Res., 127, 23, 10.1016/0006-8993(77)90378-X Ju, 1989, Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat. I. Cytoarchi tecture, J. Comp. Neurol., 280, 587, 10.1002/cne.902800409 Ju, 1989, Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat.II. Chemoarchitecture, J. Comp. Neurol., 280, 603, 10.1002/cne.902800410 Kelche, 1984, Olfactory cues and accessory olfactory bulb lesion: effects on sexual behavior in the cyclic female rat, Physiol Behav., 45, 10.1016/0031-9384(84)90011-8 Kelley, 1988, Sexually dimorphic behaviors, Annu. Rev. Neurosci., 11, 225, 10.1146/annurev.ne.11.030188.001301 Keverne, 1979, The dual olfactory projections and their signifi-cance for behaviour, 75 Keverne, 1983, Pheromonal influences on the endocrine regula tion of reproduction, TINS, 66, 381 Keverne, 1982, Pheromones in mice: Reciprocal interactions between the nose and brain, Nature, 296, 148, 10.1038/296148a0 Kevetter, 1981, Connections of the corticomedial amygdala in the golden hamster. I. Efferents of the ‘vomeronasal amygdala’, J. Comp. Neurol., 197, 81, 10.1002/cne.901970107 Kevetter, 1981, Connections of the corticome dial amygdala in the golden hamster. II. Efferents of the ‘olfac tory amygdala’, J. Comp. Neurol., 197, 99, 10.1002/cne.901970108 Kinsley, 1988, Prenatal stress and maternal behavior in intact virgin rats: response latencies are decreased inmales and increased in females, Hormones Behav., 22, 76, 10.1016/0018-506X(88)90032-3 Kondo, 1986, Recovery of lordotic activity by dorsal deafferentiation of the preoptic area in male and androgenized female rats, Physiol. Behav., 37, 495, 10.1016/0031-9384(86)90212-X Kondo, 1990, Role of septum and preoptic area in regulating masculine and feminine sexual behavior in male rats, Hormones Behav., 24, 421, 10.1016/0018-506X(90)90019-T Konishi, 1985, Birdsong: from behavior to neuron, Annu. Rev. Neurosci, 8, 125, 10.1146/annurev.ne.08.030185.001013 Konishi, 1985, Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch, Nature, 315, 145, 10.1038/315145a0 Krettek, 1978, Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat, J. Comp. Neurol., 178, 225, 10.1002/cne.901780204 Krettek, 1978, A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid connections, J. Comp. Neurol., 178, 255, 10.1002/cne.901780205 Larsson, 1964, Mating behavior of male rats after lesions in the preoptic area, Nature, 202, 413, 10.1038/202413a0 Lehman, 1982, Vomeronasal and olfactory pathways to the amygdala controlling male hamster sexual be havior: Autoradiographic and behavioral analyses, Brain Res., 240, 27, 10.1016/0006-8993(82)90641-2 Lehman, 1980, Medial nucleus of the amygdala mediates chemosensory control of male hamstersexual behavior, Science, 210, 557, 10.1126/science.7423209 Leonard, 1971, Origin and distribution of the amygdalofugal pathways in the rat: an experimental neuroanatomical study, J. Comp. Neurol., 141, 313, 10.1002/cne.901410304 Lomas, 1982, Role of vomeronasal organ and prolactin in acceleration of puberty in female mice, J. Reprod. Fert., 66, 101, 10.1530/jrf.0.0660101 López, 1982, Investigation of peripeduncular hypothalamic pathways involved in the control of lordosis in the rat, Brain Res., 253, 287, 10.1016/0006-8993(82)90696-5 Luskin, 1983, The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb, J. Comp. Neurol., 216, 264, 10.1002/cne.902160305 Mackay-Sim, 1986, Removal of the vomeronasal organ impairs lordosis in female hamsters: effect is reversed by luteinising hormone-releasing hormone, Neuroendocrinology, 42, 489, 10.1159/000124492 Malsbury, 1977, Effects of medial hypothalamic lesions on the lordosis response and other behaviors in female golden hamsters, Physiol. Behav., 19, 223, 10.1016/0031-9384(77)90331-6 Marques, 1979, Roles of the main olfactory and vomeronasal systems in the responses of the female hamster to young, Behav. Neural Biol., 26, 311, 10.1016/S0163-1047(79)91300-1 Masco, 1984, Pathways conducting amygdaloid influence on feminine sexual behavior in the rat, Behav. Brain Res., 11, 205, 10.1016/0166-4328(84)90212-2 Matsumoto, 1983, Sex difference in volume of the ventromedial nucleus of the hypothalamus in the rat, Endocrinol. Jpn., 30, 277, 10.1507/endocrj1954.30.277 Matsumoto, 1986, Male-female difference in synap tic organization of the ventromedial nucleus of the hypothala-mus in the rat, Neuroendocrinology, 42, 232, 10.1159/000124445 Mayer, 1979, Ontogeny of maternal behavior in the laboratory rat: factors underlyingchanges in responsiveness from 30 to 90 days, Dev. Psychobiol., 12, 425, 10.1002/dev.420120503 McEwen, 1991, Non-genomic and genomic effects of steroids on neural activity, TIPS, 12, 141 McShane, 1988, Cortical asymmetry — a preliminary study: neurons-glia, female-male, Exp. Neurol., 99, 353, 10.1016/0014-4886(88)90153-7 Mendelson, 1984, Cholecystokinin-octapep tide produces inhibition of lordosis in the female rat, Pharmacol. Biochem. Behav., 21, 755, 10.1016/S0091-3057(84)80015-5 Menella, 1988, Infanticide in rats: male strategy and female counter-strategy, Physiol. Behav., 42, 19, 10.1016/0031-9384(88)90254-5 Menella, 1988, Infanticide in the male rat: The role of the vomeronasal organ, Physiol. Behav., 42, 303, 10.1016/0031-9384(88)90087-X Meredith, 1980, The vomeronasal organ and accessory olfactory system in the hamster, 303 Meredith, 1983, Sensory physiology of pheromone communica tion, 199 Meredith, 1986, Vomeronasal organ removal before sexual experience impairs male hamster mating behavior, Physiol. Behav., 36, 737, 10.1016/0031-9384(86)90362-8 Meredith, 1980, Vomeronasal pump: significance for male hamster sexual behavior, Science, 207, 1224, 10.1126/science.7355286 Micevych, 1987, Distribution of cholecystokinin-immunoreactive cell bodies in the male and female rats. I. Hypothalamus, J. Comp. Neurol., 255, 124, 10.1002/cne.902550110 Micevych, 1988, Distribution of chole cystokinin-inmunoreactive cell bodies in the male and female rats. II. Bed nucleus of the stria terminalis and amygdala, J. Comp. Neurol., 269, 381, 10.1002/cne.902690306 Mizukami, 1983, Sexual difference in nuclear volume and its ontogeny in the rat amygdala, Experimental Neurol., 79, 569, 10.1016/0014-4886(83)90235-2 Mora, 1985, Role of vomeronasal organ on the estral cycle reduction by pheromones in the rat, Rev. Espahola Fisiol., 41, 305 Naess, 1976, Androgen receptors in the anterior pituitary and central nervous system of the androgen ‘insensitive’ (Tmf) rat:Correlation between receptor binding and effects of androgens on gonadotropin secretion, Endocrinology, 99, 1295, 10.1210/endo-99-5-1295 Nishizuka, 1981, Sexual dimorphism in synaptic organization in the amygdala its dependence on neonatal hormone environment, Brain Res., 212, 31, 10.1016/0006-8993(81)90029-9 Nishizuka, 1981, Organizational action of estrogen on synaptic pattern in the amygdala: implications for sexual differentiation of the brain, Brain Res., 213, 422, 10.1016/0006-8993(81)90247-X Nordeen, 1985, Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus, Science, 229, 671, 10.1126/science.4023706 Nottebohm, 1980, Testosterone triggers growth of brain vocal control nuclei in adult female canaries, Brain Res., 189, 429, 10.1016/0006-8993(80)90102-X Nottebohm, 1976, Sexual dimorphism in vocal control areas of the song bird brain, Science, 194, 211, 10.1126/science.959852 Nottebohm, 1986, Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei, Behav. Neural. Biol., 46, 445, 10.1016/S0163-1047(86)90485-1 Numan, 1988, Neural basis of maternal behavior in the rat, Psychoneuroendocrinology, 13, 47, 10.1016/0306-4530(88)90006-6 Numan, 1980, The connections of the media preoptic region and maternal behavior in the rat, Physiol. Behav., 25, 653, 10.1016/0031-9384(80)90367-4 O'Connell, 1984, Effects of volatile and non volatile chemical signals on male sex behaviors mediated by the main and accesssory systems, Behav. Neurosci., 98, 1083, 10.1037/0735-7044.98.6.1083 Ottersen, 1982, Connections of the amygdala of the rat. IV. Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase, J. Comp. Neuro., 205, 30, 10.1002/cne.902050104 Paxinos, 1986 Perkins, 1980, Effects of stimulus female on sexual behavior of male rats given olfactory tubercle and corticomedial amygdaloid lesions, Physiol. Behav., 25, 495, 10.1016/0031-9384(80)90112-2 Pfaff, 1980 Pfaff, 1973, Atlas of estradiol-concentrating cells in Central Nervous System of the female rat, J. Comp. Neurol., 151, 121, 10.1002/cne.901510204 Pfaff, 1979, Facilitation of the lordosis reflex of female rats from the ventromedial nucleus of the hypothalamus, J. Physiol., 288, 189 Pfaff, 1979, Deficit in the lordosis reflex of female rats caused by lesions in the ventromedial nucleus of the hypothalamus, J. Physiol., 288, 203 Pfaff, D.W. and Schwartz-Giblin S., Cellular Mechanisms of Female Reproductive Behaviors. In E. Knobil and J.D. Neill (Eds.), The Physiology of Reproduction, Vol. 2, Raven Press, New York, pp. 1487–1568. Pohl-Apel, 1985, The correlation between the degree of brain masculinization and song quality in estradiol treated female zebra finches, Brain Res., 336, 381, 10.1016/0006-8993(85)90673-0 Powell, 1965, The central olfactory connexions, J. Anal., 99, 791 Powers, 1972, Sexual receptivity: Facilitationby medial preoptic lesions in female rats, Science, 175, 1003, 10.1126/science.175.4025.1003 Powers, 1975, Vomeronasal organ: critical role in mediating sexual behavior of the male hamster, Science, 187, 961, 10.1126/science.1145182 Powers, 1979, Olfactory and vomeronasal system participation in male hamster attraction to female vaginal secretions, Physiol. Behav., 22, 77, 10.1016/0031-9384(79)90407-4 Price, 1973, An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex, J. Comp. Neurol., 150, 87, 10.1002/cne.901500105 Quadagno, 1972, The effect of gonadal hormones in infancy on maternal behavior in the adult rat, Hormones Behav., 3, 55, 10.1016/0018-506X(72)90007-4 Raisman, 1972, An experimental study of the projection of the amygdala to the accesssory olfactory bulb and its relationship to the concept of a dual olfactory system, Exp. Brain Res., 14, 395, 10.1007/BF00235035 Raisman, 1971, Sexual dimorphism in the preoptic area of the rat, Science, 173, 731, 10.1126/science.173.3998.731 Raisman, 1973, Sexual dimorphism in the neuropilof the preoptic area of the rat and its dependence on neonatal androgen, Brain Res., 54, 1, 10.1016/0006-8993(73)90030-9 Rajendren, 1986, Effect of bilateral transection of the lateral olfactory tract on the male-induced implantation failure (the Bruce effect) in mice, Physiol. Behav., 36, 587, 10.1016/0031-9384(86)90338-0 Ramón, 1901, Textura del lóbulo olfativo accesorio, Trab. Lab. Invest. Biol., 1, 143 Reisert, 1991, Sexual differentiation of monoamin ergic neurons — genetic or epigenetic?, TINS, 14, 468 Reynolds, 1979, The accessory olfactory system and its role in the pheromonally mediated suppression of oestrus in grouped mice, J. Reprod. Fert., 57, 31, 10.1530/jrf.0.0570031 Rhees, 1990, Onset of the hormone-sensitive perinatal period for sexual differentiation of the sexually dimorphic nucleus of the preoptic area in female rats, J. Neurobiol., 21, 781, 10.1002/neu.480210511 Rhees, 1990, Termination of the hormone-sensitive period for differentiation of the sexually dimorphic nucleus of the preoptic area in male and female rats, Dev. Brain Res., 52, 17, 10.1016/0165-3806(90)90217-M Romero, 1990, Participation of the olfactory system in the control of approach behavior of the female rat to the male, Physiol Behav., 47, 685, 10.1016/0031-9384(90)90078-I Roos, 1988, Sexual differences in the development of accessory olfactory bulbs in the rat, J. Comp. Neurol., 270, 121, 10.1002/cne.902700110 Roselli, 1985, Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system, Endocrinology, 117, 2471, 10.1210/endo-117-6-2471 Roselli, 1987, The distribution and regulation of aromatasa activity in the central nervous system, Steroids, 50, 495, 10.1016/0039-128X(87)90034-1 Ryan, 1978, Studies on the role of the medial preoptic area in sexual behavior and hormonal response to sexual behavior in the mature male laboratory rat, Biol. Reprod., 19, 971, 10.1095/biolreprod19.5.971 Sachs, B.D. and Meisel, R.L. The physiology of male sexual behavior. In E. Knobil and J.D. Neill (Eds.), The Physiology of Reproduction, Vol. 2, Raven Press, New York, pp. 1393–1485. Saito, 1986, Induction of maternal behavior in sexually unexperienced male rats following removal of the vomeronasal organ, Jpn. J. Vet. Sci., 48, 1029, 10.1292/jvms1939.48.1029 Saito, 1988, Maternal behavior in virgin female rats following removal of the vomeronasal organ, Zool. Sci., 5, 1141 Saito, 1986, Copulatory behavior of sexually naive and sexually experienced male rats following removal of the vomeronasal organ, Physiol. Behav., 37, 507, 10.1016/0031-9384(86)90215-5 Saito, 1986, Sexual behavior in the female rat following removal of the vomeronasal organ, Physiol. Behav., 38, 81, 10.1016/0031-9384(86)90135-6 Sánchez-Criado, 1979, Blockade of the pheromonal effects in rat by central deafferentiation of the accessory olfactory system, Reu. Esp. Fisiol., 35, 137 Sánchez-Criado, 1982, Involvement of the vomeronasal system in the reproductive physiology of the rat, 209 Saper, 1984, Organization of cerebral cortical afferent system in the rat. II. Magnocellular basal nucleus, J. Comp. Neurol., 222, 313, 10.1002/cne.902220302 Saper, 1976, The efferent connections of the ventromedial nucleus of the hypothalamus of the rat, J. Comp. Neurol., 169, 409, 10.1002/cne.901690403 Sar, 1972, Cellular localization of androgens in the brain and pituitary after the injection of tritiated testosterone, Experientia, 28, 1364, 10.1007/BF01965348 Sar, 1977, Distribution of androgen target cells in rat forebrain and pituitary after [3H]dihydrotestosterone admin istration, J. Comp. Neurol., 8, 1131 Sar, 1981, Central noradrenergic neurons concentrate [3H]oestradiol, Nature, 289, 500, 10.1038/289500a0 Scalia, 1975, The differential projections of the olfactory bulb and accessory olfactory bulb in mammals, J. Comp. Neurol., 161, 31, 10.1002/cne.901610105 Scalia, 1976, New perspectives on the morphol-ogy of the olfactory system: olfactory and vomeronasal pathways in mammals, 7 Schaeffer, 1986, Accessory olfactory bulb lesions and lordosis behavior in the male rat feminized with ovarian hormones, Horm. Behav., 20, 118, 10.1016/0018-506X(86)90034-6 Schumacher, 1990, Rapid membrane effects of steroid hormones: an emerging concept in neuroendocrinology, TINS, 13 Scott, 1971, The olfactory connections of the lateral hypothalamus in the rat, mouse and hamster, J. Comp. Neurol., 141, 331, 10.1002/cne.901410305 Segovia, 1982, Effects of sex steroids on the development of the vomeronasal organ in the rat, Dev. Brain Res., 5, 209, 10.1016/0165-3806(82)90160-2 Segovia, 1986, Effects of sex steroids on the development of the vomeronasal system in the rat, 35 Segovia, 1990, Age-related changes in cell population of the locus coeruleus in the rat, Med. Sci. Res., 18, 29 Segovia, 1984, Effects of sex steroids on the development of the accessory olfactory bulb in the rat: a volumetric study, Dev. Brain Res., 16, 312, 10.1016/0165-3806(84)90036-1 Segovia, 1984, Effects of postpuberal gonadectomy on the neurosensorial epithelium of the vomeronasal organ in the rat, Dev. Brain Res., 14, 289, 10.1016/0165-3806(84)90315-8 Segovia, 1991, Early diazepam exposure alters sex differences in the rat brain, Brain Res. Bull., 26, 899, 10.1016/0361-9230(91)90255-I Segovia, 1986, Effects of sex steroids on the development of two granule cell subpopulations in the accessory olfactory bulb, Dev. Brain Res., 30, 283, 10.1016/0165-3806(86)90121-5 Selmanoff, 1977, Aromatization and 5-α-reduction of androgens in discrete hypothalamic and limbic regions of the male and female rat, Endocrinology, 101, 841, 10.1210/endo-101-3-841 Shammah-Lagnado, 1981, Efferents connections of the olfactory bulb in the oppossum (Didelphis marsupialis aurita): a Fink-Heimer study, J. Comp. Neurol., 201, 51, 10.1002/cne.902010105 Shapiro, 1976, Is feminine differentiation of the brain hormonally determinated?, Experientia, 32, 650, 10.1007/BF01990214 Sheridan, 1979, The nucleus interstitialis strie terminalis and the nucleus amygdaloideus medialis: prime targets for androgen in the rat forebrain, Endorinology, 104, 130, 10.1210/endo-104-1-130 Simerly, 1990, Hormonal control of neuropeptide gene expression in sexually dimorphic olfactory pathways, TINS, 13, 104 Simerly, 1990, Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study, J. Comp. Neurol., 294, 76, 10.1002/cne.902940107 Simerly, 1986, The organization of neural inputs to the medial preoptic nucleus of the rat, J. Comp. Neurol., 246, 312, 10.1002/cne.902460304 Simerly, 1984, Demonstration of a sexual dimorphism in the distribution of serotonin inmunoreactive fibers in the medial preoptic nucleus of the ra, J. Comp. Neurol., 225, 151, 10.1002/cne.902250202 Simerly, 1985, The distribution of monoaminergic cells and fibers in a periventricular preoptic nucleus involved in the control of gonadotropin: immunohistochemical evidence for a dopaminergic sexual dimorphism, Brain Res., 330, 55, 10.1016/0006-8993(85)90007-1 Södersten, 1983, Vasopressing alters female sexual behaviour by acting on the brain independently of alterations in blood pressure, Nature, 301, 608, 10.1038/301608a0 Staudt, 1976, Structural changes in the medial and central amygdala of the male rat, following neonatal castration and androgen treatment, Endocrinology, 67, 296 Struble, 1982, Light microscopic differentiation of two populations of rat olfactory bulb granule cells, Brain Res., 236, 237, 10.1016/0006-8993(82)90711-9 Stumpff, 1982, he olfactory system as a target organ for steroid hormones, 11 Swaab, 1985, A sexually dimorphic nucleus in the human brain, Science, 228, 1112, 10.1126/science.3992248 Swaab, 1988, Sexual differentiation of the human hypothalamus: ontogeny of the sexually dimorphic nucleus of the preoptic area, Dev. Brain Res., 44, 314, 10.1016/0165-3806(88)90231-3 Swanson, 1976, An autoradiographic study on the efferent connections of the preoptic region in the rat, J. Comp. Neural., 167, 227, 10.1002/cne.901670207 Swanson, 1976, Autoradiographic studies of the development and connections of the septal area in the rat, 37 Swanson, 1979, The connections of the septal region in the rat, J. Comp. Neurol., 186, 621, 10.1002/cne.901860408 Swanson, 1975, The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-β-hydroxylase as a marker, J. Comp. Neurol., 163, 467, 10.1002/cne.901630406 Tobet, 1986, Differentiation in male ferrets of a sexually dimorphic nucleus of the preoptic/anterior hypothalamic area requires prenatal estrogen, Neuroendocrinology, 44, 299, 10.1159/000124660 Toran-Allerand, 1984, On the genesis of sexual differentiation of the central nervous system: morphogenetic consequences of steroidal exposure and possible role of α-fetoprotein, Progr. Brain Res., 61, 63, 10.1016/S0079-6123(08)64429-5 Turkenburg, 1988, Effects of lesions of the sexually dimorphic nucleus on sexual behavior of testosterone-treated female rats, Brain Res. Bull., 21, 215, 10.1016/0361-9230(88)90234-1 Turner, 1976, Projections of the nucleus and tracts of the stria terminalis following lesions at the level of the anterior commissure, Exp. Neurol., 51, 468, 10.1016/0014-4886(76)90270-3 Valcourt, 1979, Penile reflexes and copulatory behavior in male rats following lesions in the bed nucleus of the stria terminalis, Brain Res. Bull., 4, 131, 10.1016/0361-9230(79)90068-6 Valencia, 1987, Efecto de los esteroides sexuales sobre la diferenciación del bulbo olfatorio accesorio de la rata Valencia, 1986, Effects of sex steroids on the development of the accessory olfactory bulb mitral cells in the rat, Dev. Brain Res., 24, 287, 10.1016/0165-3806(86)90197-5 Valencia, 1992, Postnatal administration of dihydrotestosterone to the male rat abolishes sexual dimorphism in the accessory olfactory bulb: a volumetric study, Dev. Brain Res., 68, 132, 10.1016/0165-3806(92)90255-U Van Leeuwen, 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, 10.1016/0006-8993(85)90348-8 Viglietti-Panzica, 1986, A sexually dimorphic nucleus in the quail preoptic area, Neurosci. Lett., 64, 129, 10.1016/0304-3940(86)90087-X Ward, 1972, Prenatal stress feminizes and demasculinizes the behavior of males, Science, 175, 82, 10.1126/science.175.4017.82 Warenbourg, 1985, Steroid receptors in the brain: topography and some functional implications, Neurochem. Int., 7, 941, 10.1016/0197-0186(85)90142-1 Weller, 1982, Afferent connections to the bed nucleus of the stria terminalis, Brain Res., 232, 255, 10.1016/0006-8993(82)90272-4 Whalen, 1974, Sexual differentiation: models, methods and mechanisms, 467 Wieland, 1981, Androgen receptors from rat kidney and brain: DNA-binding proporties of wild-type and tmf mutant, J. Steroid Biochem., 14, 409, 10.1016/0022-4731(81)90350-2 Williams, 1988, The control of neuron number, Annu. Rev. Neurosci., 11, 423, 10.1146/annurev.ne.11.030188.002231 Winans, 1977, Olfactory and vomeronasal deafferentiation of male hamsters: histological and behavioral analyses, Brain Res., 126, 325, 10.1016/0006-8993(77)90729-6 Winans, 1970, Amygdaloid nucleus: new afferent input from the vomeronasal organ, Science, 170, 330, 10.1126/science.170.3955.330 Wysocki, 1979, Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction, Neurosci. Biobehav. Rev., 3, 301, 10.1016/0149-7634(79)90015-0 Wysocki, 1987, The Vomeronasal System, 125 Yamanouchi, 1985, Presence of a neural mechanism for the expression of female sexual behaviors in the male rat brain, Neuroendocrinology, 40, 393, 10.1159/000124104 Yamanouchi, 1985, Neural and hormonal control of lordosis behavior in the rat, Zool Science, 2, 617 Young, 1936, The nuclear pattern and fiber connections of the non-cortical centers of the telencephalon of the rabbit (Lepus cuniculus), J. Comp. Neurol., 65, 295, 10.1002/cne.900650112