Summary
The distribution of biogenic amines in the rat hypoglossal nucleus (nXII) was investigated with immunocytochemical methods using antibodies to tyrosine hydroxylase (TH) as a marker for catecholamines, and to 5-hydroxytryptamine (5-HT), the principal indoleamine, at the light microscopic level. TH and 5-HT immunoreactivity were found throughout all regions of nXII. Although the innervations overlapped, clearly differnt patterns of distribution were observed. TH immunoreactivity was localized primarily in the ventromedial quadrant of the caudal half of nXII and appeared largely as perisomatic-like profiles. In contrast, 5-HT immunoreactivity was greatest dorsally along the caudal half of nXII, although secondary foci of staining were evident ventrolaterally and, to a lesser extent, ventromedially. A perisomatic-like pattern of termination was observed for 5-HT in both dorsal and ventral regions of nXII. Since ventral and dorsal districts of nXII contain motoneurons that innervate protrusor and retrusor tongue muscles, respectively, we propose that the overlapping, yet differential distributions of catecholamines and indoleamines are important in controlling the relationships between functionally related groups of nXII motoneurons. These findings are discussed in relation to oro-lingual motor dysfunction.
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Aghajanian GK, McCall R (1980) Serotonergic synaptic input to facial motoneurons: localization by electron microscopic autoradiography. Neuroscience 5: 2155–2162
Aldes LD, Boone TB (1985) Organization of projections from the principal sensory trigeminal nucleus to the hypoglossal nucleus in the rat: an experimental light and electron microscopic study with axonal tracer techniques. Exp Brain Res 59: 16–29
Aldes LD, Chronister RB, Marco LA (1988) Distribution of glutamic acid decarboxylase and gamma-aminobutyric acid in the hypoglossal nucleus of the rat. J Neurosci Res 19: 343–348
Arluison M, Diehl M, Thibault J (1984) Ultrastructural morphology of dopaminergic nerve terminals and synapses in the striatum of the rat using tyrosine hydroxylase immunochemistry. A topographic study. Brain Res Bull 13: 269–285
Baldessarini RJ, Tarsy D (1980) Dopamine and the pathophysiology of dyskinesias induced by antipsychotic drugs. Ann Rev Neurobiol 3: 23–41
Barnard JW (1940) The hypoglossal complex of vertebrates. J Comp Neurol 72: 489–524
Bennett GA, Ramsey AJ (1941) Experimental studies on the movements of the mammalian tongue. Anat Rec 79: 37–39
Bole CT, Lessler MA (1966) Electromyography of the genioglossus muscles in man. J Applied Physiol 21: 1695–1698
Borke RC, Nau ME, Ringler RL Jr (1983) Brain stem afferents of hypoglossal neurons in the rat. Brain Res 269: 47–55
Bowker RM, Westlund KN, Coulter JD (1981) Origins of serotonergic projections to the spinal cord in rat: an immunocytochemical retrograde transport study. Brain Res 226: 187–199
Bowker RM, Westlund KN, Sullivan MC, Coulter JD (1982) Organization of descending serotonergic projections to the spinal cord. In: Kuypers HGJM, Martin GF (eds) Descending pathways to the spinal cord. Progress in brain research, Vol 57. Elsevier, Amsterdam, pp 239–265
Cajal y Ramon S (1909) Histologie du système nerveaux de l'homme et des vertébrates. Maloine, Paris, pp 702–711
Calza L, Giardino L, Grimaldi R, Rigoli, Steinbusch HWM, Tiengo M (1985) Presence of 5-HT-positive neurons in the medial nuclei of the solitary tract. Brain Res 347: 135–139
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
Chan-Palay V (1977) Indoleamine neurons and their processes in the normal rat brain and in chronic diet-induced thiamine deficiency demonstrated by uptake of 3H-serotonin. J Comp Neurol 176: 467–494
Chronister RB, Aldes LD (1985) Immunocytochemical, histofluorescent and histochemical characterization of the hypoglossal nucleus. Anat Rec 211: 40A
Clark RW, Schmidt HS, Schaal SF, Boudoulas H, Schuller DE (1979) Sleep apnea: treatment with protriptyline. Neurol 29: 1287–1292
Commissiong JW, Hellstrom SO, Neff NH (1978) A new projection from locus coeruleus to the spinal ventral columns: histochemical and biochemical evidence. Brain Res 148: 207–213
Conway WA, Zorick F, Piccione P and Roth T (1982) Protriptyline in the treatment of sleep apnoea. Thorax 37: 49–53
Dahlström A, Fuxe K (1964) Evidence for the existence of monoamine containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brainstem neurons. Acta Physiol Scand (Suppl) 62: 1–55
Ermini EB, Aldes LD (1988) Differential organization of rat parabrachial-hypoglossal projections. Anat Rec (in press)
Gaudin-Chazal G, Portalier P, Barrit MC, Puizillout JJ (1982) Serotonin-like immunoreactivity in paraffin-sections of the nodose ganglia of the cat. Neurosci Lett 33: 169–172
Gerlach J (1979) Tardive dyskinesia. Dan Med Bull 26: 209–245
Gregg RA, Carpenter DO (1982) Responses of hypoglossal motoneurons to various neurotransmitters in a brain slice preparation. Soc Neurosci Abstr 8: 958
Haycock JW, Waymire JC (1982) Activating antibodies to tyrosine hydroxylase. J Biol Chem 257: 9416–9423
Holtman JR, Norman WP, Gillis RA (1984) Projections from the raphe nuclei to the phrenic motor nucleus in the cat. Neurosci Lett 44: 105–111
Holtman JR, Dick TE, Berger AJ (1986) Involvement of serotonin in the excitation of phrenic motoneurons evoked by stimulation of the raphe obscurus. J Neurosci 6: 1185–1193
Jones BE, Yang TZ (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 242: 56–92
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
Kattwinkel J, Mars H, Fanaroff MB, Klaus MH (1976) Urinary biogenic amines in idiopathic apnea of prematurity. J Pediat 88: 1003–1006
Klawans HL (1973) The pharmacology of tardive dyskinesia. Am J Psychiat 130: 82–85
Krammer EB, Rath T, Lischka MF (1979) Somatotopic organization of the hypoglossal nucleus: an HRP study in the rat. Brain Res 170: 533–537
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
Levitt P, Moore RY (1979) Origin and organization of brainstem catecholamine innervation in the rat. J Comp Neurol 186: 505–528
Lewis PR, Flumerfelt BA, Shute CCD (1971) The use of cholinesterase techniques to study topographical localisation in the hypoglossal nucleus of the rat. J Anat (Lond) 110: 203–213
Lorente de Nó R (1947) Action potential of the motoneurons of the hypoglossal. nucleus. J Cell Comp Physiol 29: 207–287
Lowe AA (1978) Excitatory and inhibitory inputs to hypoglossal motoneurons and adjacent reticular neurons in cats. Exp Neurol 62: 30–47
Maurizi CP (1985) Could supplementary dietary tryptophan prevent sudden infant death syndrome? Med Hypoth 17: 149–154
McCall RB, Aghajanian GK (1979) Serotonergic facilitation of facial motoneuron excitation. Brain Res 169: 11–27
Mizukawa K, Otsuka N, Hattori T (1986) Serotonin-containing nerve fibers in the rat spinal cord: electron microscopic immunohistochemistry. Acta Med Ikayama 40: 1–10
Mizuno N, Sauerland EK (1970) Trigeminal proprioceptive projections to the hypoglossal nucleus and the cervical ventral gray column. J Comp Neurol 139: 215–226
Morimoto T, Takata M, Kawamura Y (1968) Effect of lingual nerve stimulation on hypoglossal motoneurons. Exp Neurol 22: 174–190
Nagatsu T, Levitt M, Udenfriend S (1964) Tyrosine hydroxylase: the initial step in norepinephrine biosynthesis. J Biol Chem 239: 2910–2917
Nygren LG, Olson L (1977) A new major projection from locus coeruleus: the main source of noradrenergic nerve terminals in the ventral and dorsal columns of the spinal cord. Brain Res 132: 85–93
Odutola AB (1976) Cell grouping and Golgi architecture of the hypoglossal nucleus of the rat. Exp Neurol 52: 356–371
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
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, Australia
Pazos A, Palacios JM (1985) Quantitative autoradiographic mapping of serotonin receptors in the rat brain. I. Serotonin-1 receptors. Brain Res 346: 205–230
Pazos A, Cortes R, Palacios JM (1985) Quantitative autoradiographic mapping of serotonin receptors in the rat brain. II. Serotonin-2 receptors. Brain Res 346: 231–249
Pickel VM, Chan J, Park TH, Milner TA (1986) Ultrastructural localization of phenylethanolamine N-methyltransferase in sensory and motor nuclei of the vagus nerve. J Neurosci Res 15: 439–455
Renfroe JB, Chronister RB, Haycock JW, Waymire JC (1984) The localization of tyrosine hydroxylase-like immunoreactivity in the central nervous system: methodological considerations. Brain Res Bull 13: 109–126
Ricardo JA, Koh ET (1978) Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Res 153: 1–26
Romanes GJ (1981) Cunningham's textbook of anatomy, 12th edn. Oxford University Press, Oxford, pp 296–297
Saavedra JM (1977) Distribution of serotonin and synthesizing enzymes in discrete areas of the brain. Fed Proc 36: 2134–2141
Saper CB, Loewy AD (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res 197: 291–317
Scheibel ME, Scheibel AB (1958) Structural substrates for integrative patterns in the brain stem reticular core. In: Jasper HH, Proctor LD (eds) Reticular formation of the brain. Little Brown, New York, pp 31–55
Scheibel ME, Scheibel AB (1970) Organization of spinal motoneuron dendrites in bundles. Exp Neurol 28: 106–112
Smith PL, Haponik EF, Allen RP, Bleecker ER (1983) The effects of protriptyline in sleep-disordered breathing. Am Rev Respir Dis 127: 8–13
Steinbusch HWM (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat — cell bodies and terminals. Neuroscience 6: 557–618
Sternberger LA (1979) The unlabeled antibody peroxidase-antiperoxidase (PAP) method. In: Immunocytochemistry. J Wiley, New York, pp 104–169
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
Szentágothai J (1948) Anatomical considerations of monosynaptic reflex arcs. J Neurophysiol 11: 445–454
Takeuchi Y, Kojima M, Matsuura T, Sano Y (1983) Serotonergic innervation on the motoneurons in the mammalian brainstem. Anat Embryol 167: 321–333
Thibault J, Vidal D, Gros F (1981) In vitro translation of mRNA from rat pheochromocytoma tumors. Characterization of tyrosine hydroxylase. Biochem Biophys Res Comm 99: 960–968
Tokado M, Yamamoto T, Hirose G (1982) On the supranuclear controls of the hypoglossal nucleus: a morphological study. Brain Nerve 34: 129
Travers JB, Norgren R (1983) Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220: 280–298
Vacca LL, Abrahams SJ, Naftchi NE (1980) A modified peroxidase-antiperoxidase procedure for improved localiation of tissue antigens: localization of substance P in rat spinal cord. J Histochem Cytochem 28: 297–307
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
Westlund KN, Coulter JD (1980) Descending projections of the locus coeruleus and subcoeruleus/medial parabrachial nuclei in monkey: axonal transport studies and dopamine-B-hydroxylase immunocytochemistry. Brain Res Reviews 2: 235–264
Westlund KN, Bowker RM, Ziegler MG, Coulter JD (1982) Descending noradrenergic projections and their spinal terminations. In: Kuypers HGJM, Martin GF (eds) Descending pathways to the spinal cord, progress in brain research, Vol 57. Elsevier, Amsterdam, pp 219–238
Westlund KN, Bowker RM, Ziegler MG, Coulter JD (1983) Noradrenergic projections to the spinal cord of the rat. Brain Res 263: 15–31
White SR, Neuman RS (1980) Facilitation of spinal motoneurone excitability by 5-hydroxytryptamine and noradrenaline. Brain Res 188: 119–127
White SR, Neuman RS (1983) Pharmacological antagonism of facilitatory but not inhibitory effects of serotonin and norepinephrine on excitability of spinal motoneurons. Neuropharmacology 2: 489–494
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Aldes, L.D., Chronister, R.C., Marco, L.A. et al. Differential distribution of biogenic amines in the hypoglossal nucleus of the rat. Exp Brain Res 73, 305–314 (1988). https://doi.org/10.1007/BF00248222
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DOI: https://doi.org/10.1007/BF00248222