Summary
Development of dopaminergic neurons was investigated in dissociated cell cultures raised from the diencephalon of male and female rat fetuses from days 14 and 17 of gestation. Striking differences in morphology and function of male and female dopaminergic neurons were observed. Outgrowth of tyrosine hydroxylase-immunoreactive processes initially proceeded at a faster rate in female than in male cultures. Morphological differences disappeared in cultures of gestational day 17. Irrespective of the age of the cultures and of the length of cultivation, the uptake capacity for (3H)dopamine per immunoreactive neuron was twice as high in female than in male cultures. Treatment of the cultures with sex steroids did not influence morphology, numbers, or transmitter uptake of tyrosine hydroxylase-immunoreactive neurons. The results suggest that diencephalic dopaminergic systems exhibit a sexual dimorphism that develops unexpectedly early in ontogeny and is independent of the action of gonadal hormones.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
references
Ahnert-Hilger G, Engele J, Reisert I, Pilgrim Ch (1986) Different developmental schedules of dopaminergic and noradrenergic neurons in dissociation culture of fetal rat midbrain and hindbrain. Neuroscience 17:157–165
Arnold AP, Gorski RA (1984) Gonadal steroid induction of structural sex differences in the central nervous system. Ann Rev Neurosci 7:413–442
Bunney BS, Sesack SR, Silva NL (1987) Midbrain dopaminergic systems: Neurophysiology and electrophysiological pharmacology. In: Meltzer HY (ed) Psychopharmacology: The Third Generation of Progress. Raven Press, New York, pp 113–126
Coyle JT (1977) Biochemical aspects of neurotransmission in the developing brain. Int Rev Neurobiol 20:65–103
Coyle JT, Snyder SH (1969) Antiparkinsonian drugs: Inhibition of dopamine uptake in the corpus striatum as a possible mechanism of action. Science 166:899–901
Demarest KT, McKay DW, Reigle GD, Moore KD (1981) Sexual differences in tuberoinfundibular dopamine activity induced by neonatal androgen exposure. Neuroendocrinology 32:108–113
Engele J, Pilgrim Ch, Reisert I (1987) Nigrostriatal dopaminergic neurons in culture are sexually dimorphic. Neuroscience 22:S235
Engele J, Pilgrim Ch, Kirsch M, Reisert I (1989) Different developmental potentials of diencephalic and mesencephalic dopaminergic neurons in vitro. Brain Res (in press)
Flügge G, Wuttke W, Fuchs E (1986) Postnatal development and sexual differentiation of central nervous catecholaminergic systems. Biogenic Amines 3:249–255
Gangnerau M-N, Picon R (1987) Onset of steroidogenesis and differentiation of functional LH receptors in rat fetal testicular cultures. Arch Androl 18:215–224
Gorski RA, Jacobson CD (1982) Sexual differentiation of the brain. Front Horm Res 10:1–14
Hagino N, Inoue K (1986) Hypothalamic dopamine may play a role in inducing prolactin in pituitary cells. Int J Dev Neurosci 4:119–128
Langer SZ, Raisman R, Briley M (1981) High-affinity (3H)DMI binding is associated with neuronal noradrenaline uptake in the periphery and the central nervous system. Eur J Pharmacol 72:423–424
Lee C-M, Snyder SH (1981) Norepinephrine neuronal uptake binding sites in rat brain membranes labeled with (3H)desipramine. Proc Natl Acad Sci USA 78:5250–5254
MacLusky NJ, Naftolin F (1981) Sexual differentiation of the central nervous system. Science 211:1294–1303
McEwen BS (1981) Neural gonadal steroid actions. Science 211:1303–1311
McEwen BS, Parsons B (1982) Gonadal steroid action on the brain: Neurochemistry and neuropharmacology. Ann Rev Pharmacol Toxicol 22:555–598
Moore KE (1987) Hypothalamic dopaminergic neuronal systems. In: Meltzer HY (ed) Psychopharmacology: The Third Generation of Progress. Raven Press, New York, pp 127–139
Noumura T, Weisz J, Lloyd CW (1966) In vitro conversion of 7-3H-progesterone to androgens by the rat testis during the second half of fetal life. Endocrinology 78:245–253
Prochiantz A, Di Porzio U, Kato A, Berger B, Glowinski J (1979) In vitro maturation of mesencephalic dopaminergic neurons from mouse embryos is enhanced in presence of their striatal target cells. Proc Natl Acad Sci USA 76:5387–5391
Puymirat J, Barret A, Faivre-Bauman A, Tixier-Vidal A (1987) Biochemical characterization of the uptake and release of (3H)dopamine by dopaminergic hypothalamic neurons: A developmental study using serum-free medium cultures. Dev Biol 119:75–84
Reisert I, Han V, Lieth E, Toran-Allerand D, Pilgrim Ch, Lauder J (1987) Sex steroids promote neurite growth in mesencephalic tyrosine hydroxylase immunoreactive neurons in vitro. Int J Dev Neurosci 5:91–98
Rohrer H, Acheson AL, Thibault J, Thoenen H (1986) Developmental potential of quail dorsal root ganglion cells analyzed in vitro and in vivo. J Neurosci 6:2616–2624
Sar M (1984) Estradiol is concentrated in tyrosine hydroxylasecontaining neurons of the hypothalamus. Science 223:938–940
Simerly RB, Swanson LW, Gorski RA (1985a) The distribution of monoaminergic cells and fibers in a periventricular preoptic nucleus involved in the control of gonadotropin release: Immunohistochemical evidence for a dopaminergic sexual dimorphism. Brain Res 330:55–64
Simerly RB, Swanson LW, Handa RJ, Gorski RA (1985b) Influence of perinatal androgen on the sexually dimorphic distribution of tyrosine hydroxylase-immunoreactive cells and fibers in the anteroventral periventricular nucleus of the rat. Neuroendocrinology 40:501–510
Tennyson VM, Barrett RE, Cohen G, Coté L, Heikkila R, Mytilineou C (1972) The developing neostriatum of the rabbit: Correlation of fluorescence histochemistry, electron microscopy, endogenous dopamine levels, and (3H)dopamine uptake. Brain Res 46:251–285
Toran-Allerand CD (1984) On the genesis of sexual differentiation of the central nervous system: Morphogenetic consequences of steroidal exposure and possible role of alpha-fetoprotein. In: De Vries GJ, De Bruin JPC, Uylings HBM, Corner MA (eds) Progress in Brain Research, Vol 61, Eisevier, Amsterdam, pp 63–98
Unsicker K, Reichert-Preibsch H, Schmidt R, Pettmann B, Labourdette G, Sensenbrenner M (1987) Astroglial and fibroblast growth factors have neurotrophic functions for cultured peripheral and central nervous system neurons. Proc Natl Acad Sci USA 84:5459–5463
Vaccari A, Brotman S, Cimino J, Timiras PS (1977) Sex differentiation of neurotransmitter enzymes in central and peripheral nervous systems. Brain Res 132:176–185
Wai-Sum O, Short RV, Renfree MB, Shaw G (1988) Primary genetic control of somatic sexual differentiation in a mammal. Nature 331:716–717
Warren DW, Haltmeyer GC, Eik-Nes KB (1973) Testosterone in the fetal rat testis. Biol Reprod 8:560–565
Weisz J, Ward IL (1980) Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology 106:306–316
Wilson WE, Agrawal AK (1979) Brain regional levels of neurotransmitter amines as neurochemical correlates of sex-specific ontogenesis in the rat. Dev Neurosci 2:195–200
Wong DT, Horng JS, Bymaster FP, Hauser KL, Molloy BB (1974) A selective inhibitor of serotonin uptake: Lilly 110140, 3-(ptrifluoromethylphenoxy)-N-methyl-3-phenylpropylamine. Life Sci 15:471–479
Yen SSC (1980) Neuroendocrine regulation of the menstrual cycle. In: Krieger DT, Hughes JC (eds) Neuroendocrinology. Sinauer Ass. Inc., Sunderland, Mass.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Reisert, I., Engele, J. & Pilgrim, C. Early sexual differentiation of diencephalic dopaminergic neurons of the rat in vitro. Cell Tissue Res. 255, 411–417 (1989). https://doi.org/10.1007/BF00224125
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00224125