Summary
The noradrenergic terminals in the substantia gelatinosa of the dorsal horn of the cervical spinal cord of the rat were investigated by means of the histofluorescence technique and electron-microscopic cytochemistry using the glyoxylic acid-KMnO4 fixation technique. In accordance with the topographical distribution of fluorescent catecholaminergic fibers, noradrenergic terminals containing small granular vesicles were frequently observed electron microscopically in the outer layer of the substantia gelatinosa. These terminals were most frequently found to appose without showing typical synaptic features, small-caliber dendrites, spine apparatus, and rarely, large caliber dendrites. Only in a few cases, the noradrenergic terminals exhibited typical synaptic contacts with dendritic elements of small size. In addition, noradrenergic terminals apposed non-noradrenergic terminals containing small agranular vesicles. In rats bearing surgical lesions of the dorsal roots, no noradrenergic terminal were found in contact with the degenerated axon terminals in the substantia gelatinosa. These findings suggest that the noradrenergic afferents to the substantia gelatinosa may exert their influence on sensory transmission via dorsal horn cells.
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Ajika K, Hökfelt T (1973) Ultrastructural identification of catecholamine neurons in the hypothalamic periventricular-arcuate nucleus-median eminence complex with special reference to quantitative aspects. Brain Res 57:97–117
Akil H, Liebeskind JC (1975) Monoaminergic mechanisms of stimulation produced analgesia. Brain Res 94:279–296
Andén N-E, Jukes MGM, Lundberg A, Vyklicky L (1966) The effect of DOPA on the spinal cord. 1. Influence on transmission from primary afferents. Acta Physiol Scand 67:373–386
Barbar R, Saito K (1976) Light microscopic visualization of GAD and GABA-T in immunohistochemical preparations of rodent CNS. In: Roberts E, Chase TN, Tower DB (eds) GABA in nervous system function. Raven Press, New York, 113–132
Basbaum AI, Fields HL (1979) The origin of descending pathways in the dorsolateral funiculus of the spinal cord of the cat and rat: Further studies on the anatomy of pain modulation. J Comp Neurol 187:513–532
Beal JA (1979) Serial reconstruction of Ramón y Cajal's large primary afferent complexes in laminae II and III of the adult monkey spinal cord: A Golgi study. Brain Res 166:161–165
Beal JA, Fox CA (1976) Afferent fibers in the substantia gelatinosa of the adult monkey (Macaca mulatta): A Golgi study. J Comp Neurol 168:113–144
Beattie MS, Bresnahan JC, King JS (1978) Ultrastructural identification of dorsal root primary afferent terminal after anterograde filling with horseradish peroxidase. Brain Res 153:127–134
Belcher G, Ryall RW, Schaffner R (1978) The differential effect of 5-hydroxytryptamine, noradrenaline and raphe stimulation on nociceptive and non-nociceptive dorsal horn interneurons in the cat. Brain Res 151:307–321
Björklund A, Skagerberg G (1979) Evidence for a major spinal cord projection from diencephalic A 11 dopamine cell group in the rat using transmitter-specific fluorescent retrograde tracing. Brain Res 177:170–175
Bloom FE (1973) Ultrastructural identification of catecholamine-containing central synaptic terminals. J Histochem Cytochem 21:333–348
Bloom FE, Hoffer BJ, Siggins GR (1971) Studies on norepinephrine-containing afferents to Purkinje cells of rat cerebellum. I. Localization of the fibers and their synapses. Brain Res 25:501–521
Bodnar RJ, Ackermann RF, Kelly DD, Glusman M (1977) Elevations in nociceptive threshold following locus coeruleus lesion. Brain Res Bull 3:125–130
Coimbra A, Sodré-Borges BP, Magalhães MM (1974) The substantia gelatinosa Rolandi of the rat. Fine structure, cytochemistry (acid phosphatase) and changes after dorsal root section. J Neurocytol 3:199–217
Commissiong JW, Hellström SO, Neff NH (1978) A new projection from locus coeruleus to the spinal ventral columns: Histochemical and biochemical evidence. Brain Res 148:207–213
Dahlström A, Fuxe K (1965) Evidence for the existence of monoamine-containing neurons in the central nervous system. II. Experimentally induced changes in the intraneuronal amine levels of bulbospinal neuron systems. Acta Physiol Scand 64, Suppl 247:1–36
Descarries L, Droz B (1970) Intraneuronal distribution of exogenous norepinephrine in the central nervous system of the rat. J Cell Biol 44:385–399
Descarries L, Lapierre Y (1973) Noradrenergic axon terminals in the cerebral cortex of rat. I. Radioautographic visualization after topical application of DL-[3H]norepinephrine. Brain Res 51:141–160
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
Dubuisson D, Wall PD (1980) Descending influences on receptive fields and activity of single units recorded in laminae 1,2 and 3 of cat spinal cord. Brain Res 199:283–298
Duncan D, Morales R (1978) Relative numbers of several types of synaptic connections in the substantia gelatinosa of the cat spinal cord. J Comp Neurol 182:601–610
Engberg I, Ryall RW (1966) The inhibitory action of noradrenaline and other monoamines on spinal neurons. J Physiol 185:298–322
Fuxe K (1965) Evidence for the existence of monoamine containing neurons in the central nervous system. IV. The distribution of monoamine terminals in the central nervous system. Acta Physiol Scand 64, Suppl 24:39–85
Guyenet PG (1980) The coerulospinal noradrenergic neurons: Anatomical and electrophysiological studies in the rat. Brain Res 189:121–133
Halász N, Ljungdahl Å, Hökfelt T (1978) Transmitter histochemistry of the rat olfactory bulb. II. Fluorescence histochemical, autoradiographic and electron microscopic localization of monoamines. Brain Res 154:253–271
Headley PM, Duggan AW, Giersmith BT (1978) Selective reduction by noradrenaline and 5- hydroxytryptamine of nociceptive responses of cat dorsal horn neurons. Brain Res 145:185–189
Heimer L, Wall PD (1968) The dorsal root distribution of the substantia gelatinosa of the rat with a note on the distribution in the cat. Exp Brain Res 6:89–99
Hicks TP, McLennan H (1978) Actions of octopamine upon dorsal horn neurons of the spinal cord. Brain Res 157:402–406
Hodge CJ, Woods CI, Delatizky J (1979) The effect of L-DOPA on dorsal horn cell responces to innocuous skin stimulation. Brain Res 173:271–285
Hodge CJ, Apkarian AV, Stevens R, Vogelsang G, Wisnicki HJ (1981) Locus coeruleus modulation of dorsal horn unit responces to cutaneous stimulation. Brain Res 203:415–420
Hökfelt T (1967) On the ultrastructural localization of noradrenaline in the central nervous system of the rat. Z Zellforsch 79:110–117
Hökfelt T (1968) In vitro studies on central and peripheral monoamine neurons at the ultrastructural level. Z Zellforsch 91:1–74
Hökfelt T, Kellerth JO, Nilsson G, Pernow B (1975) Substance P: Localization in the central nervous system and in some primary sensory neurons. Science 190:889–890
Hökfelt T, Elde RV, Johansson O, Luft R, Nilsson R, Arimura A (1976) Immunocytochemical evidence for separate populations of somatostatin-containing and substance P-containing primary afferent neurons in the rat. Neuroscience 1:131–136
Hökfelt T, Ljungdahl A, Terenius L, Elde R, Nilsson G (1977) Immunohistochemical analysis of peptide pathways possibly related to pain and analgesia: Enkephalin and substance P. Pro Natl Acad Sci 74:3081–3085
Hökfelt T, Terenius L, Kuypers HGJM, Dann O (1979) Evidence for enkephalin immunoreactive neurons in the medulla oblongata projecting to the spinal cord. Neurosci Lett 14:55–60
Kimoto Y, Tohyama M, Satoh K, Sakumoto T, Takahashi Y, Shimizu N (1981) Fine structure of rat cerebellar noradrenaline terminals as visualized by potassium permanganate “in situ perfusion” fixation method. Neuroscience 6:47–58
Kimura H, Tohyama M, Maeda T, Shimizu N (1976) A stable modified histofluorescence method using glyoxylic acid. Acta Histochem Cytochem 9:98
Kimura H, Kashiba A, Amano S, Imamoto K, Maeda T (1978) Electron microscopic observation of endogenous amine in the CNS demonstrated by “Glyoxylic acid-Mg++-KMnO4 fixation method”. Acta Anat Nipponica 53:62–63
Kimura H, McGeer PL, Peng JH, McGeer EG (1981a) The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J Comp Neurol 200:151–201
Kimura H, Satoh K, Kashiba A, Maeda T (1981b) A detailed methodology for central aminergic systems under the electron microscope by using GA-KMnO4 fixation: In comparison with the aldehyde fixation method, (in preparation)
Koda LY, Bloom FE (1977) A light and electron microscopic study of noradrenergic terminals in the rat dentate gyrus. Brain Res 120:327–335
Koda LY, Schulman JA, Bloom FE (1978) Ultrastructural identification of noradrenergic terminals in rat hippocampus: Unilateral destruction of the locus coeruleus with 6-hydroxydopamine. Brain Res 145:190–195
Landis SC, Bloom FE (1975) Ultrastructural identification of noradrenergic boutons in mutant and normal mouse cerebellar cortex. Brain Res 96:299–305
Leichnetz GR, Watkins L, Griffin G, Murfin R, Mayer DJ (1978) The projection from raphe magnus and other brainstem nuclei to the spinal cord in the rat: A study using the HRP blue-reaction. Neurosci Lett 8:119–124
Maeda T, Kashiba A, Tohyama M, Hori M, Itakura T, Shimizu N (1975) Demonstration of aminergic terminals and their contacts in rat brain by perfusion fixation with potassium permanganate. Proc Xth Int Cong Anat, Tokyo (abstract)
Mayer DJ, Price DD (1976) Central nervous system mechanisms of analgesia. Pain 2:379–404
Melzack R, Wall PD (1965) Pain mechanisms: A new theory. Science 150:971–979
Mendell LM (1966) Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol 16:316–331
Nagy JI, Vincent SR, Staines WMA, Fibiger HC, Reisine TD, Yamamura HI (1980) Neurotoxic action of capsaicin on spinal substance P neurons. Brain Res 186:435–444
Nygren L-G, 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
Otsuka M, Konishi S (1976) GABA in the spinal cord. In: Roberts E, Chase TN, Tower DB (eds) GABA in nervous system function. Raven Press, New York, 197–202
Ralston HJ (1965) The organization of the substantia gelatinosa Rolandi in the cat lumbosacral spinal cord. Z Zellforsch 67:1–23
Ralston HJ (1968a) The fine structure of neurons in the dorsal horn of the cat spinal cord. J Comp Neurol 132:275–302
Ralston HJ (1968b) Dorsal root projections to dorsal horn neurons in the cat spinal cord. J Comp Neurol 132:391–401
Reddy SVR, Yaksh TL (1980) Spinal noradrenergic terminal system mediate antinociception. Brain Res 189:391–401
Réthelyi M (1977) Preterminal and terminal axon arborizations in the substantia gelatinosa of cat's spinal cord. J Comp Neurol 172:511–528
Réthelyi M, Szentágothai J (1969) The large synaptic complexes of the substantia gelatinosa. Exp Brain Res 7:258–274
Ruda MA, Gobel S (1980) Ultrastructural characterization of axonal endings in the substantia gelatinosa which take up 3H serotonin. Brain Res 184:57–83
Sakumoto T (1980) Morphological and histochemical studies on the neurons of the hypothalamic paraventricular nucleus projecting to the spinal cord. In: Yoshida S, Share Scientific Societies Press, Tokyo, and University Park Press, Baltimore, p 33–50
Sakumoto T, Tohyama M, Satoh K, Itakura T, Yamamoto K, Kinugasa T, Tanizawa O, Kurachi K, Shimizu N (1977) Fine structure of noradrenaline containing nerve fibers in the median eminence of female rat demonstrated by in situ fixation of potassium permangenate. J Hirnforsch 18:521–530
Sar M, Stumpf WE, Miller RJ, Chang K-J, Cuatrecasas P (1978) Immunohistochemical localization of enkephalin in rat brain and spinal cord. J Comp Neurol 182:17–38
Satoh K, Tohyama M, Yamamoto K, Sakumoto T, Shimizu N (1977) Noradrenaline innervation of the spinal cord studied by the horseradish peroxidase method combined with monoamine oxidase staining. Exp Brain Res 30:175–186
Satoh M, Kawarajiri S, Ukai Y, Yamamoto M (1979) Selective and nonselective inhibition by enkephalin and noradrenaline of nociceptive response of lamina V type neuron in the spinal dorsal horn of the rabbit. Brain Res 177:384–387
Shimizu N, Katoh Y, Hida T, Satoh K (1979) The fine structural organization of the locus coeruleus in the rat with reference to noeradrenaline contents. Exp Brain Res 37:139–148
Steiner TJ, Turner LM (1972) Cytoarchitecture of the rat spinal cord. J Physiol (Lond) 222:123–125
Swanson LW, Mckellar S (1979) The distribution of oxytocin and neurophysin-stained fibers in the spinal cord of the rat and monkey. J Comp Neurol 188:87–106
Swanson LW, Connelly MA, Hartman BK (1978) Further studies on the fine structure of the adrenergic innervation of the hypothalamus. Brain Res 151:165–174
Szentágothai J (1964) Neuronal and synaptic arrangement in the substantia gelatinosa Rolandi. J Comp Neurol 122:219–239
Takahashi T, Otsuka M (1975) Regional distribution of substance P in the spinal cord and nerve roots of the cat and the effect of dorsal root section. Brain Res 87:1–11
Takahashi Y, Tohyama M, Satoh K, Sakumoto T, Kashiba Y, Shimizu N (1980) Fine structure of noradrenaline nerve terminals in the dorsomedial portion of the nucleus tractus solitarii as demonstrated by modified potassium permanganate method. J Comp Neurol 189:525–535
Wall PD (1980) The role of the substantia gelatinosa as a gate control. In: Bronica JJ (ed) Pain. Research publications: Association for research in nervous and mental disease, vol 58, Raven Press, New York, 205–231
Watson SJ, Akil H, Sullivan S, Barchas JD (1977) Immunocytochemical localization of methionine enkephalin: Preliminary observation. Life Science 21:733–738
Wood KG, McLaughlin BJ, Vaughn JE (1976) Immunocytochemical localization of GAD in electron microscopic preparations of rodent CNS. In: Roberts E, Chase TN, Tower DB (eds) GABA in nervous system function. Raven Press, New York, 133–148
Yaksh TL (1979) Direct evidence that spinal serotonin and noradrenaline terminals mediate the spinal antinociceptive effects of morphine in the periaqueductal gray. Brain Res 160:180–185
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Satoh, K., Kashiba, A., Kimura, H. et al. Noradrenergic axon terminals in the substantia gelatinosa of the rat spinal cord. Cell Tissue Res. 222, 359–378 (1982). https://doi.org/10.1007/BF00213218
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DOI: https://doi.org/10.1007/BF00213218