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Visceral Afferent Projections to the Thoracolumbar Spinal Cord in Normal and Capsaicin-Treated Rats

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The Primary Afferent Neuron

Abstract

Among the primary afferents projecting to the spinal cord, visceroafferent neurons represent a small but substantial population (Jänig and Morrison, 1986). Although their percentage, i.e., around 10% or even less of all afferent neurons in the main segments of entry, seems to be low as compared to somatic afferents (Cervero et al., 1984; Neuhuber et al., 1986), the effects elicited by visceroafferent stimulation are widespread and of well-known clinical significance (Jänig and Morrison, 1986; Procacci et al., 1986; Cervero, 1988; Ness and Gebhart, 1988).

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References

  • Abrahams, V.C., Richmond, F.J., and Keane, J., 1984, Projections from C2 and C3 nerves supplying muscles and skin of the cat neck: A study using transganglionic transport of horseradish peroxidase, J. Comp Neurol., 230:142–154

    Article  PubMed  CAS  Google Scholar 

  • Baron, R., Jänig, W., and Kollmann, W., 1988, Sympathetic and afferent somata projecting in hindlimb nerves and the anatomical organization of the lumbar sympathetic nervous system of the rat, J. Comp. Neurol., 275:460–468

    Article  PubMed  CAS  Google Scholar 

  • Carlton, S.M., McNeill, D.L., Chung, K., and Coggeshall, R.E., 1988, Organization of calcitonin gene-related peptide-immunoreactive terminals in the primate dorsal horn, J. Comp. Neurol., 276:527–536

    Article  PubMed  CAS  Google Scholar 

  • Caverson, M.M., Ciriello, J., and Calaresu, F.R., 1983, Direct pathway from cardiovascular neurons in the ventrolateral medulla to the region of the intermediolateral nucleus of the upper thoracic cord: an anatomical and electrophysiological investigation in the cat, J. Autonom. Nerv. Syst., 9:451–475

    Article  CAS  Google Scholar 

  • Cechetto, D.F., Standaert, D.G., and Saper, C.B., 1985, Spinal and trigeminal dorsal horn projections to the parabrachial nucleus in the rat, J. Comp. Neurol., 240:153–160

    Article  PubMed  CAS  Google Scholar 

  • Cervero, F., 1983, Somatic and visceral inputs to the thoracic spinal cord of the cat: Effects of noxious stimulation of the biliary system, J. Physiol. (Lond.), 337:51–67

    CAS  Google Scholar 

  • Cervero, F., 1988, Neurophysiology of gastrointestinal pain, Bailliere’s Clin. Gastroenterol., 2:183–199

    Article  CAS  Google Scholar 

  • Cervero, F., and Connell, L.A., 1984a, Distribution of somatic and visceral primary afferent fibers within the thoracic spinal cord of the cat, J. Comp. Neurol., 230:88–98

    Article  CAS  Google Scholar 

  • Cervero, F., and Connell, L.A., 1984b, Fine afferent fibers from viscera do not terminate in the substantia gelatinosa of the thoracic spinal cord, Brain Res., 294:370–374

    Article  CAS  Google Scholar 

  • Cervero, F., Connell, L.A., and Lawson, S.N., 1984, Somatic and visceral primary afferents in the lower thoracic dorsal root ganglia of the cat, J. Comp. Neurol., 228:422–431

    Article  PubMed  CAS  Google Scholar 

  • Cervero, F., and McRitchie, H.A., 1982, Neonatal capsaicin does not affect unmyelinated efferent fibers of the autonomic nervous system: Functional evidence, Brain Res., 239:283–288

    Article  PubMed  CAS  Google Scholar 

  • Changgeng, Z., Zenker, W., and Celio, M.R., 1983, Substance P-positive structures in rat spinal cord. A longitudinal bundle ventral to the central canal, Anat. Anz., 154:193–203

    PubMed  CAS  Google Scholar 

  • Ciriello, J., and Calaresu, F.R., 1983, Central projections of afferent renal fibers in the rat: an anterograde transport study of horseradish peroxidase, J. Autonom. Nerv. Syst., 8:273–285

    Article  CAS  Google Scholar 

  • Craig, A.D., and Mense, S., 1983, The distribution of afferent fibers from the gastrocnemius-soleus muscle in the dorsal horn of the cat, as revealed by the transport of horseradish peroxidase, Neurosci. Lett., 41:233–238

    Article  PubMed  CAS  Google Scholar 

  • Crousillat, J., Ranieri, F., and Perrin, J., 1979, Interactions entre afférences somatiques et viscérales le long de la voie sensitive splanchnicque, Arch. Ital. Biol., 117:186–188

    Google Scholar 

  • Csillik, B., and Knyihar-Csillik, E., 1986, “The protean gate”, Akademiai Kiadó, Budapest

    Google Scholar 

  • Dalsgaard, C.-J., Hökfelt, T., Elfvin, L.-G., Skirboll, L., and Emson, P., 1982, Substance P-containing primary sensory neurons projecting to the inferior mesenteric ganglion: evidence from combined retrograde tracing and immunohistochemistry, Neuroscience, 7:647–654

    Article  PubMed  CAS  Google Scholar 

  • Dalsgaard, C.-J., Ygge, J., Vincent., S.R., Ohrling, M., Dockray, G.J., and Eide, R., 1984, Peripheral projections and neuropeptide coexistence in a subpopulation of fluoride-resistant acid phosphatase reactive spinal primary sensorx neurons, Neurosci. Lett., 51:139–144

    Article  PubMed  CAS  Google Scholar 

  • DeGroat, W.C., 1986, Spinal cord projections and neuropeptides in visceral afferent neurons, in: “Visceral sensation; Progress in Brain Research, Vol. 67,” F. Cervero and J.F.B. Morrison, eds., Elsevier, Amsterdam: 165–187

    Chapter  Google Scholar 

  • DeGroat, W.C., Nadelhaft, I., Morgan, C., and Schauble, T., 1978, Horseradish peroxidase tracing of visceral efferent and primary afferent pathways in the cat’s sacral spinal cord using benzidine processing, Neurosci. Lett., 10:103–108

    Article  CAS  Google Scholar 

  • Dockray, G.J., and Sharkey, K.A., 1986, Neurochemistry of visceral afferent neurons, in: “Visceral sensation: Progress in Brain Research, Vol. 67,” F. Cervero and J.F.B. Morrison, eds., Elsevier, Amsterdam: 133–148

    Chapter  Google Scholar 

  • Felpel, L.P., and Huffman, R.D., 1986, Response of splanchnic-driven neurons to substance P and eledoisin-related peptide, J. Autonom. Nerv. Syst., 15:269–274

    Article  CAS  Google Scholar 

  • Fulwiler, C.F., and Saper, C.B., 1984, Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat, Brain Res. Rev., 7:229–259

    Article  Google Scholar 

  • Giesler, Jr., G.J., Menetrey, D., and Basbaum, A.I., 1979, Differential origins of spinothalamic tract projections to medial and lateral thalamus in the rat, J. Comp. Neurol., 184:107–126

    Article  PubMed  Google Scholar 

  • Gokin, P., Kostyuk, P.-G., and Preobrazhensky, N.-N., 1977, Neuronal mechanisms of interactions of high-threshold visceral and somatic afferent influences in spinal cord and medulla, J. Physiol. (Paris), 73:319–333

    CAS  Google Scholar 

  • Granum, S.L., 1986, The spinothalamic system of the rat. I. Locations of cells of origin, J. Comp. Neurol., 247:159–180

    Article  PubMed  CAS  Google Scholar 

  • Green, T., and Dockray, G.J., 1987, Calcitonin gene-related peptide and substance P in afferents to the upper gastrointestinal tract in the rat, Neurosci. Lett., 76:151–156

    Article  PubMed  CAS  Google Scholar 

  • Hökfelt, T., Johansson, O., Kellerth, J.-O., Ljungdahl, A., Nilsson, G., Nygards, A., and Pernow, B., 1977, Immunohistochemical distribution of substance P, in: “Substance P,” U.S. von Euler and B. Pernow, eds., Raven Press, New York: 117–145

    Google Scholar 

  • Irminger, D.C., 1989, Zentrale Verteilung viszeraler Primärafferenzen in neonatal capsaicin-behandelten Ratten, Inaugural-Dissertation, Universität Zürich

    Google Scholar 

  • Jancsó, G., Hökfelt, T., Lundberg, J.M., Kiraly, E., Halasz, N., Nilsson, G., Terenius, L., Rehfeld, J., Steinbusch, H., Verhofstad, A., Eide, R., Said, S., and Brown, M., 1981, Immunohistochemical studies on the effect of capsaicin on spinal and medullary peptide and monoamine neurons using antisera to substance P, gastrin/CCK, somatostatin, VIP, enkephalin, neurotensin and 5-hydroxytryptamine, J. Neurocytol., 10:963–980

    Article  PubMed  Google Scholar 

  • Jancsó, G., Kiraly, E., Such, G., Joo, F., and Nagy, A., 1987, Neurotoxic effect of capsaicin in mammals, Acta Physiol. Hung., 69:295–313

    PubMed  Google Scholar 

  • Jancsó, G., and Maggi, C.A., 1987, Distribution of capsaicin-sensitive urinary bladder afferents in the rat spinal cord, Brain Res., 418:371–376

    Article  PubMed  Google Scholar 

  • Jänig, W., and Morrison, J.F.B., 1986, Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception, in: “Visceral sensation; Progress in Brain Research, Vol. 67,” F. Cervero and J.F.B. Morrison, eds., Elsevier, Amsterdam:87–114

    Chapter  Google Scholar 

  • Jordan, D., and Spyer, K.M., 1986, Brainstem integration of cardiovascular and pulmonary afferent activity, in: “Visceral sensation; Progress in Brain Research, Vol. 67,” F. Cervero and J.F.B. Morrison, eds., Elsevier, Amsterdam:295–314

    Chapter  Google Scholar 

  • Kuo, D.C., and DeGroat, W.C., 1985, Primary afferent projections of the major splanchnic nerve to the spinal cord and gracile nucleus of the cat, J. Comp. Neurol., 231:421–434

    Article  PubMed  CAS  Google Scholar 

  • Kuo, D.C., Nadelhaft, I., Hisamitsu, T., and DeGroat, W.C., 1983, Segmental distribution and central projections of renal afferent fibers in the cat studied by transganglionic transport of horseradish peroxidase, J. Comp. Neurol., 216:162–174

    Article  PubMed  CAS  Google Scholar 

  • Kuo, D.C., Oravitz, J. J., and DeGroat, W.C., 1984, Tracing of afferent and efferent pathways in the left inferior cardiac nerve of the cat using retrograde and transganglionic transport of horseradish peroxidase, Brain Res., 321:111–118

    Article  PubMed  CAS  Google Scholar 

  • Lawson, S.N., 1987, The morphological consequences of neonatal treatment with capsaicin on primary afferent neurones in adult rats, Acta Physiol. Hung., 69:315–321

    PubMed  CAS  Google Scholar 

  • Leah, J., Menetrey, D., and dePommery, J., 1988, Neuropeptides in long ascending spinal tract cells in the rat: evidence for parallel processing of ascending information, Neuroscience, 24:195–207

    Article  PubMed  CAS  Google Scholar 

  • Lembeck, F., and Skofitsch, G., 1982, Visceral pain reflex after pretreatment with capsaicin and morphine, Naunyn Schmiedeberg’s Arch. Pharmacol., 321:116–122

    Article  CAS  Google Scholar 

  • Lima, D., and Coimbra, A., 1983, The neuronal population of the marginal zone (lamina I) of the rat spinal cord. A study based on reconstructions of serially sectioned cells, Anat. Embryol., 167:273–288

    Article  PubMed  CAS  Google Scholar 

  • Lima and Coimbra, A., 1985, Marginal neurons of the rat spinal cord at the origin of a spinobulboreticular projection, Neurosci. Lett. Suppl.22:S9

    Google Scholar 

  • Lima, D., and Coimbra, A., 1986, Agolgi study of the neuronal population of the marginal zone (lamina I) of the rat spinal cord, J. Comp. Neurol., 244:53–71

    Article  PubMed  CAS  Google Scholar 

  • Lima, D., and Coimbra, A., 1988, The spinothalamic system of the rat: Structural types of retrogradely labelled neurons in the marginal zone (lamina I), Neuroscience, 27:215–230

    Article  PubMed  CAS  Google Scholar 

  • Lima, D., and Coimbra, A., 1989, Morphological types of spinomesencephalic neurons in the marginal zone (lamina I) of the rat spinal cord, as shown after retrograde labelling with cholera toxin subunit B, J. Comp. Neurol., 279:327–339

    Article  PubMed  CAS  Google Scholar 

  • Lindh, B., Dalsgaard, C.-J., Elfvin, L.-G., Hökfelt, T., and Cuello, A.C., 1983, Evidence of substance P immunoreactive neurons in dorsal root ganglia and vagal ganglia projecting to the guinea-pig pylorus, Brain Res., 269:365–369

    Article  PubMed  CAS  Google Scholar 

  • Liu, R.P.C., 1983, Laminar origins of spinal projection neurons to the periaqueductal gray of the rat, Brain Res., 264:118–122

    Article  PubMed  CAS  Google Scholar 

  • Mei, N., 1983, Sensory structures in the viscera, in: “Progress in Sensory Physiology, Vol. 4,” D. Ottoson, ed., Springer, Berlin: 1–42

    Google Scholar 

  • Menétrey, D., and Basbaum, A.I., 1987, Spinal and trigeminal projections to the nucleus of the solitary tract: A possible substrate for somatovisceral and viscerovisceral reflex activation, J. Comp. Neurol., 255:439–450

    Article  PubMed  Google Scholar 

  • Menétrey, D., Chaouch, A., Binder, D., and Besson, J.M., 1982, The origin of the spinomesencephalic tract in the rat: An anatomical study using the retrograde transport of horseradish peroxidase, J. Comp. Neurol., 206:193–207

    Article  PubMed  Google Scholar 

  • Menétrey, D., Roudier, F., and Besson, J.M., 1983, Spinal neurons reaching the lateral reticular nucleus as studied in the rat by retrograde transport of horseradish peroxidase, J. Comp. Neurol., 220:439–452

    Article  PubMed  Google Scholar 

  • Mesulam, M.-M., and Brushart, T.M., 1979, Transganglionic and anterograde transport of horseradish peroxidase across dorsal root ganglia: A tetramethylbenzidine method for tracing central sensory connections of muscles and peripheral nerves, Neuroscience, 4:1107–1117

    Article  PubMed  CAS  Google Scholar 

  • Miller, K.E., and Seybold, V.S., 1989, Comparison of met-enkephalin, dynorphin A, and neurotensin immunoreactive neurons in the cat and rat spinal cords: II. Segmental differences in the marginal zone, J. Comp. Neurol., 279:619–628

    Article  PubMed  CAS  Google Scholar 

  • Molander, C., Ygge, J., and Dalsgaard, C.-J., 1987, Substance P-, somatostatin-, and calcitonin gene-related peptide-like immunoreactivity and fluoride resistant acid phosphatase-activity in relation to retrogradely labeled cutaneous, muscular and visceral primary sensory neurons in the rat, Neurosci. Lett., 74:37–42

    Article  PubMed  CAS  Google Scholar 

  • Morgan, C., DeGroat, W.C., and Nadelhaft, I., 1986a, The spinal distribution of sympathetic preganglionic and visceral primary afferent neurons that send axons into the hypogastric nerves of the cat, J. Comp. Neurol., 243:23–40

    Article  CAS  Google Scholar 

  • Morgan, C., Nadelhaft, I., and DeGroat, W.C., 1981, The distribution of visceral primary afferents from the pelvic nerve to Lissauer’s tract and the spinal gray matter and its relationship to the sacral parasympathetic nucleus, J. Comp. Neurol., 201:415–440

    Article  PubMed  CAS  Google Scholar 

  • Morgan, C., Nadelhaft, I., and DeGroat, W.C., 1986b, The distribution within the spinal cord of visceral primary afferent axons carried by the lumbar colonic nerve of the cat, Brain Res., 398:11–17

    Article  CAS  Google Scholar 

  • Nadelhaft, I., and Booth, A.M., 1984, The location and morphology of preganglionic neurons and the distribution of visceral afferents from the rat pelvic nerve: A horseradish peroxidase study, J. Comp. Neurol., 226:238–245

    Article  PubMed  CAS  Google Scholar 

  • Nadelhaft, I., and McKenna, K.E., 1987, Sexual dimorphism in sympathetic preganglionic neurons of the rat hypogastric nerve, J. Comp. Neurol., 256:308–315

    Article  PubMed  CAS  Google Scholar 

  • Nadelhaft, I., Roppolo, J., Morgan, C., and DeGroat, W.C., 1983, Parasympathetic preganglionic neurons and visceral primary afferents in monkey sacral spinal cord revealed following application of horseradish peroxidase to pelvic nerve, J. Comp. Neurol., 216:36–52

    Article  PubMed  CAS  Google Scholar 

  • Nagy, J.I., and Hunt, S.P., 1983, The termination of primary afferents within the rat dorsal horn: Evidence for rearrangement following capsaicin treatment, J. Comp. Neurol., 218:145–158

    Article  PubMed  CAS  Google Scholar 

  • Ness, T.J., and Gebhart, G.F., 1988, Colorectal distension as a noxious visceral stimulus: physiologic and pharmacologic characterization of pseudoaffective reflexes in the rat, Brain Res., 450:153–169

    Article  PubMed  CAS  Google Scholar 

  • Neuhuber, W., 1982, The central projections of visceral primary afferent neurons of the inferior mesenteric plexus and hypogastric nerve and the location of the related sensory and preganglionic sympathetic cell bodies in the rat, Anat. Embryol., 164:413–425

    Article  PubMed  CAS  Google Scholar 

  • Neuhuber, W.L., Sandoz, P.A., and Fryscak, T., 1986, The central projections of primary afferent neurons of greater splanchnic and intercostal nerves in the rat. A horseradish peroxidase study, Anat. Embryol., 174:123–144

    Article  PubMed  CAS  Google Scholar 

  • Ohmori, Y., Watanabe, T., and Fujioka, T., 1987, Projections of visceral and somatic primary afferents to the sacral spinal cord of the domestic fowl revealed by transganglionic transport of horseradish peroxidase, Neurosci. Lett., 74:175–179

    Article  PubMed  CAS  Google Scholar 

  • Pomeranz, B., Wall, P.D., and Weber, W.V., 1968, Cord cells responding to fine myelinated afferents from viscera, muscle and skin, J. Physiol. (Lond.), 199:511–532

    CAS  Google Scholar 

  • Procacci, P., Zoppi, M., and Maresca, M., 1986, Clinical approach to visceral sensation, in: “Visceral sensation; Progress in Brain Research, Vol. 67,” F. Cervero and J.F.B. Morrison, eds., Elsevier, Amsterdam:21–28

    Chapter  Google Scholar 

  • Rethelyi, M., Salim, M.Z., and Jancsó, G., 1986, Altered distribution of dorsal root fibers in the rat following neonatal capsaicin treatment, Neuroscience, 18:749–761

    Article  PubMed  CAS  Google Scholar 

  • Rosenfeld, M.G., Mermod, J.J., Amara, S.G., Swanson, L.W., Sawchenko, P.E., Rivier, J., Vale, W.W., and Evans, R.M.,1983, Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing, Nature, 304:129–135

    Article  PubMed  CAS  Google Scholar 

  • Ruch, T.C., 1947, Visceral sensation and referred pain, in: “Howell’s Textbook of Physiology, 15th ed.,” J.F. Fulton, ed., Saunders, Philadelphia:385–401

    Google Scholar 

  • Sepulveda, L., and Nadelhaft, I., 1986, Preganglionic and sensory neurons of the rat greater splanchnic nerve: distribution and morphology, Neurosci. Abstr., 12:1174

    Google Scholar 

  • Sharkey, K.A., Sobrino, J.A., and Cervero, F., 1987, Evidence for a visceral afferent origin of substance P-like immunoreactivity in lamina V of the rat thoracic spinal cord, Neuroscience, 22:1077–1083

    Article  PubMed  CAS  Google Scholar 

  • Sharkey, K. A., Williams, R.G., and Dockray, G.J., 1984, Sensory substance P innervation of the stomach and pancreas. Demonstration of capsaicin-sensitive sensory neurons in the rat by combined immunohistochemistry and retrograde tracing, Gastroenterology, 87:914–921

    PubMed  CAS  Google Scholar 

  • Standaert, D.G., Watson, S.J., Houghten, R.A., and Saper, C.B., 1986, Opioid peptide immunoreactivity in spinal and trigeminal dorsal horn neurons projecting to the parabrachial nucleus in the rat, J. Neurosci., 6:1220–1226

    PubMed  CAS  Google Scholar 

  • Su, H.C., Bishop, A.E., Power, R.F., Hamada, Y., and Polak, J.M., 1987, Dual intrinsic and extrinsic origins of CGRP- and NPY-immunoreactive nerves of rat gut and pancreas, J. Neurosci., 7:2674–2687

    PubMed  CAS  Google Scholar 

  • Swett, J.E., McMahon, S.B., and Wall, P.D., 1985, Long ascending projections to the midbrain from cells of lamina I and nucleus of the dorsolateral funiculus of the rat spinal cord, J. Comp. Neurol., 238:401–416

    Article  PubMed  CAS  Google Scholar 

  • Willis, Jr., W.D., 1986, Visceral inputs to sensory pathways in the spinal cord, in: “Visceral sensation; Progress in Brain Research, Vol. 67”, F. Cervero and J.F.B. Morrison, eds., Elsevier, Amsterdam:207–225

    Chapter  Google Scholar 

  • Ygge, J., and Grant, G., 1983, The organization of the thoracic spinal nerve projection in the rat dorsal horn demonstrated with transganglionic transport of horseradish peroxidase, J. Comp. Neurol., 216:1–9

    Article  PubMed  CAS  Google Scholar 

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  1. Anatomisches Institut, Universität Zürich-Irchel, Zürich, Switzerland

    Winfried L. Neuhuber & Dominique Irminger

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  1. Winfried L. Neuhuber
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  1. Institute of Anatomy, University of Zurich-Irchel, Zurich, Switzerland

    Wolfgang Zenker  & Winfried L. Neuhuber  & 

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Neuhuber, W.L., Irminger, D. (1990). Visceral Afferent Projections to the Thoracolumbar Spinal Cord in Normal and Capsaicin-Treated Rats. In: Zenker, W., Neuhuber, W.L. (eds) The Primary Afferent Neuron. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0579-8_15

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