Abstract
Previous [3H]thymidine studies in Nisslstained sections in rats established that the substantia nigra pars compacta and the ventral tegmental area originate sequentially according to an anterolateral to posteromedial neurogenetic gradient. We investigated whether that same pattern is found in mice in the dopaminergic neurons in each of these structures. Using tyrosine hydroxylase immunostaining combined with [3H]thymidine autoradiography, the time of origin of dopaminergic midbrain neurons in the retrorubral field, the substantia nigra pars compacta, the ventral tegmental area, and the interfascicular nucleus was determined in postnatal day 20 mice. The dams of the experimental animals were injected with [3H]thymidine on embryonic days (E) 11–E12, E12–E13, E13–E14, and E14–E15. The time of origin profiles for each group indicated significant differences between populations. The retrorubral field and the substantia nigra pars compacta arose nearly simultaneously and contained the highest proportion of neurons, 49 to 37%, generated on or before E11. Progressively fewer early-generated neurons were found in the ventral tegmental area (20%), and the interfascicular nucleus (8.5%). In addition, anterior dorsolateral neurons in the substantia nigra and ventral tegmental area were more likely to be generated early than the posterior ventromedial neurons. These findings indicate that mouse and rat brains have nearly identical developmental patterns in the midbrain, and neurogenetic gradients in dopaminergic neurons are similar to those found in Nissl studies in rats.
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References
Altman J, Bayer SA (1981) Development of the brain stem in the rat. V. Thymidine-radiographic study of the time of origin of neurons in the midbrain tegmentum. J Comp Neurol 198:677–716
Bayer SA (1984) Neurogenesis in the rat neostriatum. Int J Dev Neurosci 2:163–175
Bayer SA, Altman J (1987) Directions in neurogenetic gradients and patterns of anatomical connections. Prog Neurobiol 29:57–106
Bayer SA, Altman J (1995) Neurogenesis and neuronal migration. In: Paxinos G (ed) The rat nervous system, 2nd edn, Academic Press, San Diego, pp 1041–1078
Bayer SA, Altman J, Russo RJ, Zhang X (1993) Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14:83–144
Bayer SA, Wills KV, Triarhou LC, Thomas JD, and Ghetti B (1995) Systematic differences in time of dopaminergic neuron origin between normal mice and homozygous weaver mutants. Exp Brain Res 105:200–208
Beckstead RM, Domesick VB, Nauta WJH (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 175:191–217
Carter DA, Fibiger HC (1977) Ascending projections of presumed dopamine-containing neurons in the ventral tegmentum of the rat as determined by horseradish peroxidase. Neuroscience 2:569–576
Chronister RB, Sikes RW, Wood J, DeFrance JF (1980) The pattern of termination of ventral tegmental afferents into nucleus accumbens: an anterograde HRP analysis. Neurosci Lett 17:231–235
Gerfen CR, Herkenham M, Thibault J (1987) The neostriatal mosaic. II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J Neurosci 7:3915–3934
German DC, Manaye KF (1993) Midbrain dopaminergic neurons (nuclei A8, A9, and A10): three-dimensional reconstruction in the rat. J Comp Neurol 331:297–309
Golden GS (1972) Embryologic demonstration of a nigrostriatal projection in the mouse. Brain Res 44:278–282
Groenewegen HJ, Becker NEHM, Lohman AHM (1980) Subcortical afferents of the nucleus accumbens septi in the cat, studied with retrograde axonal transport of horseradish peroxidase and bisbenzimid. Neuroscience 5:1903–1916
Hökfelt T, Skirboll L, Rehfeld JF, Goldstein M, Markey K, Dann O (1980) A subpopulation of mesencephalic dopamine neurons projecting to limbic areas contains a cholecystokinin-like peptide: evidence from immunohistochemistry combined with retrograde tracing. Neuroscience 5:2093–2124
Kalivas PW, Miller JS (1984) Neurotensin neurons in ventral tegmental area project to medial nucleus accumbens. Brain Res 300:157–160
Kalsbeek A, Buijs, RM, Hofman MA, Matthijssen MAH, Pool CW, Uylings HBM (1987) Effects of neonatal thermal lesioning of the mesocortical dopaminergic projection on the development of the rat prefrontal cortex. Dev Brain Res 32:123–132
Kalsbeek A, Feenstra MGP, van Galen H, Uylings HBM (1989) Monoamine and metabolite levels in the prefrontal cortex and the mesolimbic forebrain following neonatal lesions of the ventral tegmental area. Brain Res 479:339–343
Nauta WJH, Smith GP, Faull RLM, Domesick VB (1978) Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience 3:385–401
Newman R, Winans SS (1980) An experimental study of the ventral striatum of the golden hamster. I. Neuronal connections of the nucleus accumbens. J Comp Neurol 191:167–192
Olson L, Seiger Å (1972) Early prenatal ontogeny of central monoamine neurons in the rat: fluorescence histochemical observations. Z Anat Entwickl Gesch 137:301–316
Olson L, Seiger Å, Fuxe K (1972) Heterogeneity of striatal and limbic dopamine innervation: highly fluorescent islands in developing and adult rats. Brain Res 44:283–288
Rothman TP, Specht LA, Joh TH, Teitelman G, Pickel VM, Gershon MJ, Reis DJ (1980) Catecholamine biosynthetic enzymes are expressed in replicating cells of peripheral but not central nervous system. Proc Natl Acad Sci USA 77:621–625
Schwab M, Agid Y, Glowinski L, Thoenen H (1977) Retrograde transport of 125I-tetanus toxin as a tool for tracing fiber connections in the central nervous system. Connections of the rostral part of the rat neostriatum. Brain Res 126:211–224
Shults CW, Hashimoto R, Brady RM, Gage FH (1990) Dopaminergic cells align along radial glia in the developing mesencephalon of the rat. Neuroscience 38:427–436
Sidman RL, Angevine JB, Taber Pierce E (1971) Atlas of the mouse brain and spinal cord. Harvard University Press, Cambridge, Mass
Specht LA, Pickel VM, Joh TH, Reis DJ (1981a) Light microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. J Comp Neurol 199:233–253
Specht LA, Pickel VM, Joh TH, Reis DJ (1981b) Light microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. II. Late ontogeny. J Comp Neurol 199:255–276
Tennyson VM, Barrett RE, Cohen G, Côté 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
Triarhou LC, Norton J, Ghetti B (1988) Mesencephalic dopamine cell deficit involves areas A8, A9 and A10 in weaver mutant mice. Exp Brain Res 70:256–265
Ungerstedt U (1971) Stereotaxic mapping of the monoamine pathways in the rat brain. Acta Physiol Scand [Suppl] 367:1–29
Van Der Kooy D (1979) The organization of the thalamic, nigral and raphe cells projecting to the medial vs lateral caudate-putamen in rat. Brain Res 401:155–161
Veening JG, Cornelissen FM, Lieven PAJM (1980) The topical organization of the afferents to the caudoputamen of the rat. A horseradish peroxidase study. Neuroscience 5:1253–1268
Voorn P, Kalsbeek A, Jorritsma-Byham B, Groenewegen HJ (1988) The pre- and postnatal development of the dopaminergic cell groups in the ventral mesencephalon and the dopaminergic innervation of the striatum of the rat. Neuroscience 25:857–887
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Bayer, S.A., Wills, K.V., Triarhou, L.C. et al. Time of neuron origin and gradients of neurogenesis in midbrain dopaminergic neurons in the mouse. Exp Brain Res 105, 191–199 (1995). https://doi.org/10.1007/BF00240955
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DOI: https://doi.org/10.1007/BF00240955