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Catecholamine-containing axon terminals in the hypoglossal nucleus of the rat: an immuno-electronmicroscopic study

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Summary

A correlative light and electron microscopic investigation was undertaken to determine the morphology and distribution of catecholamine (CA)-containing axon terminals in the hypoglossal nucleus (XII) of the rat. This was accomplished immunocytochemically with antibody to tyrosine hydroxylase (TH). The major findings in this study were the following: 1) Immunoreactive profiles were found throughout XII and included unmyelinated axons, varicosities, axon terminals and dendrites; 2) Nonsynaptic immunoreactive profiles (preterminal axons, varicosities) were more frequently observed (55.2%) than synaptic profiles (43.5%); 3) CA-containing axon terminals ending on dendrites were more numerous (71.8%) than those synapsing on somata (25.4%) or nonlabeled axon terminals (2.7%); 4) The morphology of labeled axon terminals was variable. Axodendritic terminals typically contained numerous small, round agranular vesicles, a few large dense-core vesicles and were associated with either a symmetric or no synaptic specialization, axosomatic terminals were often associated with a presynaptic membrane thickening or a symmetric synaptic specialization and contained small, round and a few elliptical-shaped vesicles, while axoaxonic synapses formed asymmetric postsynaptic specializations; and 5) CA-positive dendritic processes were identified in XII. These findings confirm the CA innervation of XII, and suggest a complex, multifunctional role for CA in controlling oro-lingual motor behavior.

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References

  • Akeyson EW, Lewis MS, Molliver ME, Grzanna R (1983) Ultrastructural demonstration of noradrenergic synapses in the rat spinal cord by dopamine-B-hydroxylase. Soc Neurosci Abstr 9:285

    Google Scholar 

  • Aldes LD, Chronister RB, Marco LA (1989) Serotonin-containing axon terminals in the hypoglossal nucleus of the rat: an immunoelectron microscopic study. Brain Res Bull 23:249–256

    Google Scholar 

  • Aldes LD, Chronister RB, Marco LA, Haycock JW, Thibault J (1988a) Differential distribution of biogenic amines in the hypoglossal nucleus of the rat. Exp Brain Res 73:305–314

    Google Scholar 

  • Aldes LD, Chronister RB, Marco LA (1988b) Distribution of glutamic-acid decarboxylase and gamma-amino butyric acid in the hypoglossal nucleus of the rat. J Neurosci Res 19:343–348

    Google Scholar 

  • Aldes LD, Chronister RB, Shelton C, Haycock JW, Marco LA, Wong DL (1988c) Catecholamine innervation of the rat hypoglossal nucleus. Brain Res Bull 21:305–312

    Google Scholar 

  • Aldes LD, Boone TB (1984) A combined flat-embedding, HRP histochemical method for correlative light and electron microscopic study of single neurons. J Neurosci Res 11:27–34

    Google Scholar 

  • Beaudet A, Descarries L (1978) The monoamine innervation of rat cerebral cortex: synaptic and nonsynaptic axon terminals. Neuroscience 3:851–860

    Google Scholar 

  • Bellinger DL, Anderson WJ, Bellinger PL, Felton DL (1984) Catecholamine innervation of cervical dendrite bundles: possible phrenic nucleus innervation. Brain Res Bull 13:701–707

    Google Scholar 

  • Boone TB, Aldes LD (1984) The ultrastructure of two distinct neuron populations in the hypoglossal nucleus of the rat. Exp Brain Res 54:321–326

    Google Scholar 

  • Brouillette RT, Thach BT (1979) A neuromuscular mechanism maintaining extrathoracic airway patency. J Appl Physiol 46:772–779

    Google Scholar 

  • Brouillette RT, Thach BT (1980) Control of genioglossus muscle inspiratory activity. J Appl Physiol 49:801–808

    Google Scholar 

  • Card JP, Riley JN, Moore RY (1986) The motor trigeminal nucleus of the rat: analysis of neuronal structure and the synaptic organization of noradrenergic afferents. J Comp Neurol 250:469–484

    Google Scholar 

  • Cajal Ramony S (1909) Histologie du systeme nerveux de l'homme et des vertebres. Maloine, Paris, pp 702–711

    Google Scholar 

  • Chan JYH, Fung SJ, Chan SHH, Barnes CD (1986) Facilitation of lumbar monosynaptic reflexes by locus coeruleus in the rat. Brain Res 369:103–109

    Google Scholar 

  • Cimarusti DL, Saito K, Vaughn JE, Barber R, Roberts E, Thomas PE (1979) Immunocytochemical localization of dopamine-B-hydroxylase in rat locus coeruleus and hypothalamus. Brain Res 162:55–67

    Google Scholar 

  • Descarries L, Watkins KC, Lapierre Y (1977) Noradrenergic axon terminals in the cerebral cortex of rat. III. Topometric ultrastructural analysis. Brain Res 133:197–222

    Google Scholar 

  • Dubner R, Sessle BJ, Storey A (1978) The neural basis of oral and facial function. Plenum, New York

    Google Scholar 

  • Elmund J, Bowman JP, Morgan RJ (1983) Vestibular influence on tongue activity. Exp Neurol 81:126–140

    Google Scholar 

  • Ermini EB, Aldes LD (1988) Differential organization of rat parabrachial-hypoglossal projections in the rat. Anat Rec 220: 35A

  • Fung SJ, Barnes CD (1981) Evidence of facilitatory coerulospinal action in lumbar motoneurons of cat. Brain Res 216:299–311

    Google Scholar 

  • Gregg RA, Carpenter DO (1982) Responses of hypoglossal motoneurons to various neurotransmitters in a brain slice preparation. Soc Neurosci Abstr 8:958

    Google Scholar 

  • Grzanna R, Chee WK, Akeyson EW (1987) Noradrenergic projections to brainstem nuclei: evidence for differential projectionsfrom noradrenergic subgroups. J Comp Neurol 263:76–91

    Google Scholar 

  • Haycock JW (1987) Stimulation-dependent phosphorylation of tyrosine hydroxylase in rat corpus striatum. Brain Res Bull 19:619–622

    Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:557–580

    Google Scholar 

  • Kalia M, Fuxe K, Goldstein M (1985) Rat medulla oblongata. II. Dopaminergic, noradrenergic (A1 and A2) and adrenergic neurons, nerve fibers, and presumptive terminal processes. J Comp Neurol 233:308–332

    Google Scholar 

  • Kojima M, Matsuura T, Tanaka A, Amagai T, Imanishi J, Sano Y (1985) Characteristic distribution of noradrenergic terminals on the anterior horn motoneurons innervating the perineal striated muscles in the rat: an immuno-electronmicroscopic study. Anat Embryol 171:267–273

    Google Scholar 

  • Levitt P, Moore RY (1979) Origin and organization of brainstem catecholamine innervation in the rat. J Comp Neurol 186:505–528

    Google Scholar 

  • Levitt M, Spector S, Sjoerdsma A, Udenfriend S (1965) Elucidation of the rate limiting step in norepinephrine biosynthesis in the perfused guinea pig. J Pharmacol Exp Ther 148:1–8

    Google Scholar 

  • Lorente de No (1947) Action potential of the motoneurons of the hypoglossal nucleus. J Cell Comp Physiol 29:207–287

    Google Scholar 

  • Lowe AA (1981) The neural regulation of tongue movements. Prog Neurobiol 15:295–344

    Google Scholar 

  • Mameli O, Tolu E (1985) Visual input to the hypoglossal nucleus. Exp Neurol 90:341–349

    Google Scholar 

  • Mameli O, Tolu E (1986) Vestibular ampullar modulation of hypoglossal neurons. Physiol Behav 37:773–775

    Google Scholar 

  • Mizukawa K, Takeuchi Y (1982) Electron microscopic investigation of monoaminergic terminals to alpha-motoneurons in the anterior horn of the cat spinal cord. Acta Med Ikayama 36:85–93

    Google Scholar 

  • Nagatsu T, Levitt M, Udenfriend S (1964) Tyrosine hydroxylase: the initial step in norephinephrine biosynthesis. J Biol Chem 239:2910–2917

    Google Scholar 

  • Odutola AB (1976) Cell grouping and Golgi architecture of the hypoglossal nucleus of the rat. Exp Neurol 52:356–371

    Google Scholar 

  • Olschowka JA, Molliver ME, Grzanna R, Rice FL, Coyle JT (1981) Ultrastructural demonstration of noradrenergic synapses in the rat central nervous system by dopamine-B-hydroxylase immunocytochemistry. J Histochem Cytochem 29:271–281

    Google Scholar 

  • Palkovits M, Jacobowitz DM (1979) Topographic atlas of catecholamine and acetylcholinesterase-containing neurons in the rat brain. II. Hindbrain (mesencephalon, rhombencephalon). J Comp Neurol 157:29–42

    Google Scholar 

  • Pasik P, Pasik T, Saavedra JP (1982) Immunocytochemical localization of serotonin at the ultrastructural level. J Histochem Cytochem 30:760–764

    Google Scholar 

  • Pickel VM, Joh TH, Reis DJ (1976) Monoamine-synthesizing enzymes in central dopaminergic, noradrenergic and serotonergic neurons: immunocytochemical localization by light and electron microscopy. J Histochem Cytochem 24:792–806

    Google Scholar 

  • Remmers JE, DeGroot WJ, Sauerland EK, Anch AM (1978) Pathogenesis of upper airway occlusion during sleep. J Appl Physiol 44:931–938

    CAS  PubMed  Google Scholar 

  • Richards JG, Tranzer JP (1970) The ultrastructural localization of amine storage sites in the central nervous system with the aid of a specific marker, 5-hydroxydopamine. Brain Res 17:463–469

    Google Scholar 

  • Sauerland EK, Mitchell SP (1970) Electromyographic activity of human genioglossus muscle in response to respiration and to positional changes of the head. Bull Los Angeles Neurol Soc 35:69–73

    Google Scholar 

  • Sauerland EK, Mitchell SP (1975) Electromyographic activity of intrinsic and extrinsic muscles of the human tongue. Texas Rep Biol Med 33:445–455

    Google Scholar 

  • Scheibel ME, Scheibel AB (1970) Organization of spinal motoneuron dendrites in bundles. Exp Neurol 28:106–112

    Google Scholar 

  • Skagerberg G, Björklund A, Lindvall O, Schmidt RH (1982) Origin and termination of the diencephalo-spinal dopamine system in the rat. Brain Res Bull 9:237–244

    Google Scholar 

  • Strahlendorf JC, Strahlendorf HK, Kingsley RE, Gintautas J, Barnes CD (1980) Facilitation of the lumbar monosynaptic reflexes by locus coeruleus stimulation. Neuropharmacology 19:225–230

    Google Scholar 

  • Swanson LW, Hartman BK (1975) The central adrenergic system: an immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-B-hydroxylase as a marker. J Comp Neurol 163:467–506

    Google Scholar 

  • Takasu N, Hashimoto PH (1988) Morphological identification of an interneuron in the hypoglossal nucleus of the rat: a combined Golgi-electron microscopic study. J Comp Neurol 271:461–471

    Google Scholar 

  • Wan XST, Trojanowski JQ, Gonatas JO, Liu CN (1982) Cytoarchitecture of the extranuclear and commissural dendrites of hypoglossal nucleus neurons as revealed by conjugation of horseradish peroxidase with cholera toxin. Exp Neurol 78:167–175

    Google Scholar 

  • White SR, Neuman RS (1980) Facilitation of spinal motoneurone excitability by 5-hydroxytryptamine and noradrenaline. Brain Res 188:119–127

    Google Scholar 

  • White SR, Neuman RS (1983) Pharmacological antagonism of facilitatory but not inhibitory effects of serotonin and norepinephrine on excitability of spinal motoneurons. Neuropharmacology 22:489–494

    Google Scholar 

  • Wohlberg CJ, Davidoff RA, Hackman JC (1986) Analysis of the responses of frog motoneurons to epinephrine and norepinephrine. Neurosci Lett 69:150–155

    Google Scholar 

  • Zivin JA, Reid LJ, Saavedra JM, Kopin IJ (1975) Quantitative localization of biogenic amines in the spinal cord. Brain Res 99:293–301

    Google Scholar 

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Aldes, L.D., Shaw, B., Chronister, R.B. et al. Catecholamine-containing axon terminals in the hypoglossal nucleus of the rat: an immuno-electronmicroscopic study. Exp Brain Res 81, 167–178 (1990). https://doi.org/10.1007/BF00230113

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