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Postnatal sequential development of dopaminergic and enkephalinergic perineuronal formations in the lateral septal nucleus of the rat correlated with local neuronal maturation

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Summary

Tyrosine-hydroxylase (TH-IR) and methionineenkephalin like immunoreactivity (MetE-IR) were analyzed in the lateral septal nucleus (LSN) of the rat from birth (PO) to adulthood. TH-IR labeled specifically the dopaminergic (DA) pericellular arrangements of the LSN, as checked by negative dopamine-β-hydroxylase and phenylethanolamine-N-methyl transferase-IR, TH-IR and Met-IR processes were present at birth in the medial LSN and extended lateralwards and caudalwards from P0 to P6 to constitute two main DA terminal fields (medial and lateral) surrounding a MetE one. Within these fields, the development of perineuronal baskets followed a similar medial to lateral sequence: DA axons first surrounded a few neuronal cell bodies at P3 in the medial part of the intermediate LSN; at P6, Met-IR axons encircled more laterally located perikarya, and only at P9, some neurons located along the ventricle in the lateral DA field became surrounded. The initial aspect of TH-IR baskets consisting of few axons surrounding the cell body rapidly evolved in a positive network encapsulating the perikaryon and long segments of the proximal dendrites, whereas MetE-IR varicosities remained restricted around the perikaryon and the initial dendritic segments. Ultrastructural study at P14 revealed numerous TH-IR and MetE-IR axosomatic and axodendritic profiles. TH-IR axosomatic varicosities exhibited asymmetrical synapses, whereas MetE-IR ones displayed rare symetrical contacts. The medio-lateral gradient of development of the perineuronal baskets was parallel to the postnatal neuronal development of the LSN as evaluated by cytological criteria: neuronal density, cell size and Nissl staining. Therefore, the formation of DA and MetE perineuronal arrangements in the LSN does not seem to be subordinate to the nature of the neurotransmitter they contain but related to the level of differentiation of their target neurons. A similar sequential set-up in the development of afferences paralleling the neuronal differentiation is discussed.

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References

  • Bayer SA (1979) The development of the septal region in the rat. 1. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 183:89–106

    Google Scholar 

  • Bayer SA (1984) Neurogenesis in the rat neostriatum. Int J Dev Neurosci 2:163–176

    Google Scholar 

  • Beauvillain JC, Poulain P, Tramu G (1983) Immunocytochemical localization of enkephalin in the lateral septum of the guineapig brain. Cell Tissue Res 228:265–276

    Google Scholar 

  • Beauvillain JC, Tramu G, Croix D, Poulain P (1985) Ultrastructural study of nerve ending containing different peptides in the median eminence, the dorsal hypothalamus and the septum. Ann Endocrinol 46:9–18

    Google Scholar 

  • Berger B, Verney C, Alvarez C (1983) Postnatal development of catecholaminergic pericellular baskets in the septal area of the Sprague Dawley rats. 5th Int Catecholamine symposium Göteborg (Sweden)

  • Berger B, Verney C, Febvret A, Vigny A, Helle KB (1985) Postnatal ontogenesis of the dopaminergic innervation in the rat anterior cingulate cortex (area 24). Immunocytochemical and catecholamine fluorescence histochemical analysis. Dev Brain Res 21:31–47

    Google Scholar 

  • Carter DA, Fibiger HC (1977) Ascending projections of presumed dopamine-containing neurons in the ventral tegmentum of the rat as demonstrated by horseradish peroxidase. Neurosci 2:569–576

    Google Scholar 

  • Cesselin F, Soubrié P, Bourgoin S, Artaut F, Reisine TD, Michelot R, Glowinski J, Hamon M (1981) In vivo release of met-enkephalin in the cat brain. Neurosci 6:301–313

    Google Scholar 

  • Gall C, Moore RY (1984) Distribution of enkephalin, substance P, tyrosine hydroxylase and 5 hydroxytryptamine immunoreactivity in the septal region of the rat. J Comp Neurol 225:212–227

    Google Scholar 

  • Gaspar P, Berger B, Alvarez C, Vigny A, Henry JP (1985) Catecholaminergic innervation of the septal area in man: Immunocytochemical study using tyrosine hydroxylase and dopamine-B-hydroxylase antibodies. J Comp Neurol 241:12–33

    Google Scholar 

  • Helle KB, Fillenz M, Stanford C, Pihl KE, Srebro B (1979) A simplified method for raising antibodies to rat dopamine-β-hydroxylase. J Neurochem 32:1351–1355

    Google Scholar 

  • Hökfelt T, Johansson O, Fuxe K, Goldstein M, Park D (1976) Immunohistochemical studies on the localization and distribution of monoamine neuron system in the rat brain. III. Three catecholamine synthetizing enzymes in the rhinencephalon. Symposium Bel Air V Genève

  • Ishikawa K, Inoue K, Tosaka H, Shimada O, Suzuki M (1984) Immunohistochemical characterization of thyrotropin-releasing hormone containing neurons in rat septum. Neuroendocrinology 39:448–452

    Google Scholar 

  • Kitahama K, Pearson J, Denoroy L, Kopp N, Ulrich J, Maeda T, Jouvet M (1985) Adrenergic neurons in human brain demonstrated by immunohistochemistry with antibodies to phenylethanolamin-N-methyl transferase (PNMT): discovery of a new group in the nucleus tractus solitarius. Neurosci Lett 53:303–308

    Google Scholar 

  • Köhler C, Chan-Palay V, Steinbush H (1982) The distribution and origin of serotonin containing fibers in the septal area: a combined immunohistochemical and fluorescent retrograde study. J Comp Neurol 209:91–111

    Google Scholar 

  • Köhler C, Eriksson LG (1984) An immunohistochemical study of somatostatin and neurotensin positive neurons in the septal nuclei of the rat brain. Anat Embryol 170:1–10

    Google Scholar 

  • Lindvall O (1975) Mesencephalic dopaminergic afferents to the lateral septal nucleus of the rat. Brain Res 87:89–95

    Google Scholar 

  • Lindvall O, Stenevi U (1978) Dopamine and noradrenaline neurons projecting to the septal area in the rat. Cell Tissue Res 190:383–407

    Google Scholar 

  • Ljungdahl A, Hökfelt T, Nilsson G, Goldstein M (1978) Distribution of substance P like immunoreactivity in the central nervous system of the rat. II. Light microscopic localization in relation to catecholamine containing neurons. Neurosci 3:945–976

    Google Scholar 

  • Meibach RC, Siegel A (1977) Efferent connections of the hippocampal formation in the rat. Brain Res 124:197–224

    Google Scholar 

  • Moore RY (1978) Catecholamine innervation of the basal forebrain. I. The septal area. J Comp Neurol 177:665–684

    Google Scholar 

  • Moore RY, Björklund A, Stenevi U (1971) Plastic changes in the adrenergic innervation of the rat septal area in response to denervation. Brain Res 33:13–35

    Google Scholar 

  • Morest DK (1969) The growth of dendrites in the mammalian brain. Z Anat Entwickl Gesch 128:290–317

    Google Scholar 

  • Mourre C, Hugues M, Lombet A, Lazdunski M (1986) Postnatal development of ionic channels in the rat brain: visualization by in vitro autoradiography. Neurosci Lett Suppl 26:S 494

  • Onteniente B, De Pommery J, Menetrey D (1986) Origine des afférences enképhalinergiques, du septum lateral chez le rat. Colloque National des Neurosciences Bordeaux (France)

  • Onteniente B, Geffard M, Calas A (1984) Ultrastructural immunocytochemical study of dopaminergic innervation of the rat lateral septum with anti-dopamine antibodies. Neurosci 13: 385–393

    Google Scholar 

  • Poulain P, Martin-Boyer L, Beauvillain JC, Tramu G (1984) Study of the efferent connections of the enkephalinergic magnocellular dorsal nucleus in the guinea-pig hypothalamus using lesions, retrograde tracing and immunocytochemistry: evidence for a projection to the lateral septum. Neurosci 11:331–343

    Google Scholar 

  • Raisman G (1969) Neuroplasticity in the septal nuclei of the adult rat. Brain Res 14:25–48

    Google Scholar 

  • Ramon Y Cajal (1911) Septum lucidum ou cloison transparente. In Histologie du système nerveux Maloine Paris TII: 783–797

  • Sakanaka M, Senba E, Shiosaka S, Takatsuki K, Inagaki S, Takagi H, Kawai Y, Hara Y, Tohyama M (1982) Evidence for the existence of enkephalin-containing pathway from the area just ventrolateral to the anterior hypothalamic nucleus to the lateral septal area of the rat. Brain Res 239:240–244

    Google Scholar 

  • Seiger A, Olson L (1973) Late prenatal ontogeny of central monoamine neurons in the rat: fluorescence histochemical observations. Z Anat Entwickl Gesch 140:281–318

    Google Scholar 

  • Sotelo C, Angaut P (1973) The fine structure of the cerebellar central nuclei in the cat. I Neurons and neuroglial cells. Exp Brain Res 16:410–430

    Google Scholar 

  • Stengaard-Pedersen K, Larsson LI (1983) Met and Leu-enkephalinergic innervation of the lateral septal nucleus. Brain Res 264:152–156

    Google Scholar 

  • Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321–353

    Google Scholar 

  • Swanson LW, Cowan WM (1976) Autoradiographic studies of the development and connections of the septal area in the rat. In: JW De France (ed) The septal nucleus. Plenum Press, New York, pp 37–64

    Google Scholar 

  • Swanson LW, Cowan WM (1977) An autoradiographic study of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172:49–84

    Google Scholar 

  • Swanson LW, Cowan WM (1979) The connections of the septal region in the rat. J Comp Neurol 186:621–656

    Google Scholar 

  • Van Eden CG, Uylings HBM (1985) Cytoarchitectonic development of the prefrontal cortex of the rat. J Comp Neurol 241:253–267

    Google Scholar 

  • Verney C, Berger B, Adrien J, Vigny A, Gay M (1982) Development of the dopaminergic innervation of the rat cerebral cortex. A light microscopic immunocytochemical study using tyrosine hydroxylase antibodies. Dev Brain Res 5:41–52

    Google Scholar 

  • Vigny A, Henry JP (1981) Bovine adrenal tyrosine hydroxylase: comparative study of native and proteolysed enzyme and their interaction with anions. J Neurochem 36:483–489

    Google Scholar 

  • Woodhams PL, Roberts GW, Polak JM, Crow TJ (1983) Distribution of neuropeptides in the limbic system of the rat, the bed nucleus of the stria terminalis, septum and preoptic area. Neurosci 8:677–703

    Google Scholar 

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Verney, C., Gaspar, P., Alvarez, C. et al. Postnatal sequential development of dopaminergic and enkephalinergic perineuronal formations in the lateral septal nucleus of the rat correlated with local neuronal maturation. Anat Embryol 176, 463–475 (1987). https://doi.org/10.1007/BF00310087

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