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Origin of the met-enkephalinergic innervation of the lateral septum in the rat

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Summary

The location of the cells giving rise to the methionine-enkephalin (Met-Enk)-ergic innervation of the lateral septal nucleus has been investigated in the rat by combining immunohistochemistry and retrograde axonal tracing. Small volumes (0.06 μl) of apo-horseradish peroxidase (Apo-HRP) conjugated to wheat-germ agglutinin (WGA) and coupled with colloidal gold particles (WGA-ApoHRP-gold) were injected into the lateral septum. The retrogradely labeled cell bodies were visualized by silver intensification of the gold particles on Vibratome sections that were subsequently processed for immunohistochemistry for Met-Enk. Cells labeled with WGA-ApoHRP-gold were observed in the septal area, throughout the hypothalamus (mainly in the perifornical and lateral nuclei) and in the mesencephalon. The localization of Met-Enk-immunoreactive cells was as previously described. With the exception of a few septal cells close to the injection site, doubly labeled cells were found only in the perifornical nucleus of the hypothalamus. Almost all perifornical magnocellular cells were doubly labeled ipsilateral to the injection site, whereas on the opposite side, only about 25% of the Met-Enk-immunoreactive cells contained WGA-ApoHRP-gold. Other brain regions containing retrogradely labeled or Met-Enk-immunoreactive cells (particularly the raphe nuclei) did not show double-labeled neurons. This study demonstrates, using a new and sensitive technique for specific neurochemical tracing of tracts, that the origin of the Met-Enk-ergic innervation of the rat lateral septal nuclei lies in the magnocellular perifornical nuclei of the hypothalamus. The precise involvement of this pathway in limbic functions remains to be determined.

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References

  • Azmitia EC, Segal M (1978) An autoradiographic analysis of the different ascending projections of the dorsal and medial raphe nuclei in the rat. J Comp Neurol 179:641–668

    Google Scholar 

  • Basbaum AI, Menétrey D (1987) Wheat germ agglutinin-apoHRP gold: a new retrograde tracer for light- and electron-microscopic single- and double-label studies. J Comp Neurol 261:306–318

    Google Scholar 

  • Beauvillain G, Poulain P, Tramu G (1983) Immunocytochemical localization of enkephalin in the lateral septum of the guineapig brain. A light- and electron-microscopic study. Cell Tissue Res 228:265–276

    Google Scholar 

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

    Google Scholar 

  • Beauvillain J-C, Mitchell V, Tramu G, Mazzuca M (1988) GABA axon terminals in synapsis with enkephalin neurons in the hypothalamus of the guinea-pig. Demonstration by a double immunocytochemistry. Brain Res (in press)

  • Carette B, Poulain P (1982) Postsynaptic inhibitory effects of Metand Leu-enkephalin on endocrine and adjacent neurones in the preoptic-septal region of the guina pig. Regul Peptides 3:125–133

    Google Scholar 

  • Follénius E, Dubois MP (1979) Différenciation immunocytologique de l'innervation hypophysaire de la carpe à l'aide de sérums anti-met-enképhaline et anti-β-endorphine. C R Acad Sci (Paris) 288:639–644

    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 

  • Glazer EJ, Steinbusch H, Verhofstad A, Basbaum AI (1981) Serotonin neurons in nucleus raphe dorsalis and paragigantocellularis of the cat contain enkephalin. J Physiol (Paris) 77:241–245

    Google Scholar 

  • Hökfelt T, Elde R, Johansson O, Terenius L, Stein L (1977) The distribution of enkephalin-immunoreactive cell bodies in the rat central nervous system. Neurosci Lett 5:25–31

    Google Scholar 

  • 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 

  • Ishikawa K, Taniguchi Y, Kurosumi K, Suzuki M (1986) Origin of septal thyrotropin-releasing hormone in the rat. Neuroendocrinology 44:54–58

    Google Scholar 

  • Kita H, Oomura V (1982a) An HRP study of the afferent connections to rat medial hypothalamic region. Brain Res Bull 8:53–62

    Google Scholar 

  • Kita H, Oomura V (1982b) An HRP study of the afferent connections to rat lateral hypothalamic region. Brain Res Bull 8:63–71

    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 

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

    Google Scholar 

  • Léger L, Charnay Y, Dubois PM, Jouvet M (1986) Distribution of enkephalin-immunoreactive cell bodies in relation to serotonin-containing neurons in the raphe nuclei of the cat: immunohistochemical evidence for the coexistence of enkephalins and serotonin in certain cells. Brain Res 362:63–73

    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. Neuroscience 3:945–976

    Google Scholar 

  • Menétrey D (1985) Retrograde tracing of neural pathways with a protein-gold complex. I. Light microscopic detection after silver intensification. Histochemistry 83:391–395

    Google Scholar 

  • Mitchell V, Beauvillain J-C, Poulain P, Mazzuca M (1988) Catecholamine innervation of enkephalinergic neurons in guinea pig hypothalamus: demonstration by an in vitro autoradiographic technique combined with a post-embedding immunogold method. J Histochem Cytochem 36:533–542

    Google Scholar 

  • Nayar R, Sirett NE, Hubbard JI (1987) Neuron response to substance P and enkephalin in rat dorso-lateral septum in vitro. Brain Res Bull 19:507–509

    Google Scholar 

  • Onténiente B, Kimura H, Maeda T (1982) Electron microscopic study of Met-enkephalin-like immunoreactivity in the rat brain. J Histochem Cytochem 30:596

    Google Scholar 

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

    Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, London

    Google Scholar 

  • Pickard GE (1985) Bifurcating axons of retinal ganglion cells terminate in the hypothalamic supra chiasmatic nucleus and the suprageniculate leaflet of the thalamus. Neurosci Lett 55:211–217

    Google Scholar 

  • Poulain P, Martin-Bouyer 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 immunohistochemistry: evidence for a projection to the lateral septum. Neuroscience 11:331–343

    Google Scholar 

  • Sakanaka M, Senba E, Shiosaka S, Takatsuki K, Inagaki S, Takagi H, Kawai Y, Hara Y, Tohyama M (1982) Evidence for the existence of an 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 

  • Saper CB, Swanson LW, Cowan WM (1978) The efferent connections of the anterior hypothalamic area of the rat, cat and monkey. J Comp Neurol 182:575–600

    Google Scholar 

  • Sar M, Stumpf W, Miller R, Chang KJ, Cuatrecasas P (1978) Immunohistochemical localization of enkephalin in rat brain and spinal cord. J Comp Neurol 182:17–38

    Google Scholar 

  • Segal M, Landis SC (1974) Afferents to the septal area of the rat studied with the method of axonal transport of horseradish peroxidase. Brain Res 82:263–268

    Google Scholar 

  • Sofroniev MV, Weindl A (1978) Projections from the parvocellular vasopressin- and neurophysin-containing neurons of the suprachiasmatic nucleus. Am J Anat 153:391–430

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

    Google Scholar 

  • Uhl GR, Goodman RR, Kuhar MJ, Childers SR, Snyder SH (1979) Immunocytochemical mapping of enkephalin and somatostatin containing cell bodies, fibers and nerve terminals in the brain stem of the rat. Brain Res 116:75–94

    Google Scholar 

  • Verney C, Gaspar P, Alvarez C, Berger B (1987) Postnatal sequential development of dopaminergic and enkephalinergic perineuronal formations in the lateral septal nucleus of the rat correlated with local neuronal maturation. Anat Embryol 176:463–470

    Google Scholar 

  • Vion-Dury J, Cupo A (1988) La transmission enképhalinergique: caractéristiques fonctionnelles et rôle physiologique. Rev Neurol (Paris) 144:1–10

    Google Scholar 

  • Wamsley JK, Young WS, Kuhar MJ (1980) Immunohistochemical localization of enkephalin in rat forebrain. Brain Res 190:153–174

    Google Scholar 

  • Watson SJ, Abil H, Sullivan S, Barchas JD (1977) Immunocytochemical localization of methionin enkephalin: preliminary observations. Life Sci 21:733–738

    Google Scholar 

  • Yamano M, Inagaki S, Kito S, Tohyama M (1985) An enkephalinergic projection from the hypothalamic paraventricular nucleus to the hypothalamic ventromedialis nucleus of the rat: an experimental immunohistochemical study. Brain Res 331:25–33

    Google Scholar 

  • Zager EL, Black ML (1985) Neuropeptides in human memory and learning processes. Neurosurgery 17:355–369

    Google Scholar 

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Onténiente, B., Menétrey, D., Arai, R. et al. Origin of the met-enkephalinergic innervation of the lateral septum in the rat. Cell Tissue Res. 256, 585–592 (1989). https://doi.org/10.1007/BF00225608

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