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Neuronal pathways in the guinea-pig lumbar sympathetic ganglia as revealed by immunohistochemistry

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Summary

Tyrosine hydroxylase (TH)- and peptide-immunoreactivity of postganglionic neurons and of nerve fibres in guinea pig lumbar paravertebral sympathetic ganglia 2–4 after transection of the communicating rami and the visceral branches, respectively, were investigated by single-and double-labelling techniques. Six subpopulations of postganglionic neurons were discriminated immunohistochemically: two cell types, which were immunoreactive to only one of the applied antisera — TH, and vasoactive intestinal polypeptide (VIP); and four cell types in which immunoreactivity was colocalized — TH/neuropeptide Y (NPY), NPY/VIP, dynorphin/α-neoendorphin and dynorphin (α-neoendorphin)/NPY. Small intensely fluorescent (SIF) cells dependent on their location exhibited differential immunobehaviour to NPY-/dynorphin-(α-neoendorphin-) and TH-antisera. Immunoreactivity to substance P (SP), calcitonin gene-related peptide (CGRP), met-enkephalin-arg-phe (MEAP) and leu-enkephalin was present in nerve fibres but not in postganglionic neurons with frequent colocalization of SP/CGRP- and MEAP/leu-enkephalin- and, sometimes leu-enkephalin/SP- and dynorphin/SP-immunoreactivity. TH-immunoreactive intraganglionic nerve fibres were numerically more increased after cutting the visceral branches, than after transection of the communicating rami. Vice versa, NPY-, VIP-, dynorphin- and α-neoendorphin-immunoreactive nerve fibres were particularly increased in number after cutting the communicating rami. Many but not all of the nerve fibres exhibited colocalization of two of these peptides. SP-, CGRP-, and enkephalin-immunoreactive nerve fibres were not visibly affected by cutting the visceral branches but virtually disappeared after lesioning the communicating rami.

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References

  • Allen JM, Polak JM, Rodrigo J, Darcy K, Bloom SR (1985) Localisation of neuropeptide-Y in nerves of the rat cardiovascular system and the effect of 6-hydroxydopamine. Cardiovasc Res 19:570–577

    PubMed  CAS  Google Scholar 

  • Bachoo MJ, Ciriello J, Polosa C (1987) Effect of preganglionic stimulation on neuropeptide-like immunoreactivity in the stellate ganglion of the cat. Brain Res 400:377–382

    Article  PubMed  CAS  Google Scholar 

  • Björklund A, Hökfelt T, Owman C (1988) The peripheral nervous system. Handbook of chemical neuroanatomy, vol 6. Elsevier, Amsterdam

    Google Scholar 

  • Bonnard C, Papermaster DS, Kraehenbuhl JP (1984) The streptavidin-biotin bridge technique: application in light and electron microscope immunocytochemistry. In: Polak JM, Varndell IM (eds) Immunolabelling for electron microscopy. Elsevier, Amsterdam, pp 95–112

    Google Scholar 

  • Chiba T (1980) Neurons and paraneurons in the sympathetic ganglion of mammals. Adv Biochem Psychopharmacol 25:133–141

    PubMed  CAS  Google Scholar 

  • Colombo M, Kummer W, Heym Ch (1987) Immunohistochemistry of opioid peptides in guinea pig paraganglia. Exp Brain Res Series 16:67–72

    Google Scholar 

  • Dalsgaard C-J, Hökfelt T, Elfvin L-G, Terenius L (1982) Enkephalin-containing sympathetic preganglionic neurons projecting to the inferior mesenteric ganglion: evidence from combined retrograde tracing and immunohistochemistry. Neuroscience 7:2039–2050

    Article  PubMed  CAS  Google Scholar 

  • Dalsgaard C-J, Hökfelt T, Schultzberg M, Lundberg JM, Terenius L, Dockray DJ, Goldstein M (1983a) Origin of peptide-containing fibres in the inferior mesenteric ganglion of the guinea pig: immunohistochemical studies with antisera to substance P, enkephalin, vasoactive intestinal polypeptide, cholecystokinin and bombesin. Neuroscience 9:191–211

    Article  PubMed  CAS  Google Scholar 

  • Dalsgaard C-J, Vincent SR, Hökfelt T, Christensson I, Terenius L (1983b) Separate origins for the dynorphin and enkephalin immunoreactive fibres in the inferior mesenteric ganglion of the guinea pig. J Comp Neurol 221:482–489

    Article  PubMed  CAS  Google Scholar 

  • Darvesh S, Nance DM, Hopkins DA, Armour JA (1987) Distribution of neuropeptide-like immunoreactivity in intact and chronically decentralized middle cervical and stellate ganglia of dogs. J Auton Nerv Syst 21:167–180

    Article  PubMed  CAS  Google Scholar 

  • Della NG, Papka RE, Furness JB, Costa M (1983) Vasoactive intestinal peptide-like immunoreactivity in nerves associated with the cardiovascular system of guinea pigs. Neuroscience 9:605–619

    Article  PubMed  CAS  Google Scholar 

  • Edvinsson L, Emson P, McCulloch J, Tatemoto K, Uddman R (1983) Neuropeptide Y: cerebrovascular innervation and vasomotor effects in the cat. Neurosci Lett 43:79–84

    Article  PubMed  CAS  Google Scholar 

  • Fleminger G, Ezra E, Kilpatrick EL, Udenfriend S (1983) Processing of enkephalin-containing peptides in isolated bovine adrenal chromaffin granules. Proc Natl Acad Sci USA 80:6418–6421

    Article  PubMed  CAS  Google Scholar 

  • Forssmann W-G (1981) General methods in transmission electron microscopy of the nervous system. In: Heym C, Forssmann W-G (eds) Techniques in neuroanatomical research. Springer, Berlin Heidelberg New York, pp 21–40

    Google Scholar 

  • Gibbins IL, Furness JB, Costa M, MacIntyre I, Hillyard CJ, Girgis S (1985) Co-localization of calcitonin gene-related peptide-like immunoreactivity with substance P in cutaneous, vascular and visceral sensory neurons of guinea pigs. Neurosci Lett 57:125–130

    Article  PubMed  CAS  Google Scholar 

  • Gibbins IL, Morris JL (1987a) Co-existence of neuropeptides in sympathetic, cranial autonomic and sensory neurons innvervating the iris of the guinea pig. J Auton Nerv Syst 21:67–82

    Article  PubMed  CAS  Google Scholar 

  • Gibbins IL, Morris JL (1987b) Four immunohistochemically identifiable populations of neurons containing opioid peptides in the facial skin of guinea pigs. Neurosci Lett 27[Suppl]:575

    Google Scholar 

  • Gibbins IL, Morris JL, Furness JB, Costa M (1987a) Chemical coding of autonomic neurons. Exp Brain Res Series 16:23–27

    Google Scholar 

  • Gibbins IL, Wattchow D, Coventry B (1987b) Two immunohistochemically identified populations of calcitonin gene-related peptide (CGRP)-immunoreactive axons in human skin. Brain Res 414:143–148

    Article  PubMed  CAS  Google Scholar 

  • Grillo MA (1965) Synaptic morphology in the superior cervical ganglion of the rat before and after preganglionic denervation. J Cell Biol 27:136A

    Google Scholar 

  • Heym Ch, Kummer W (1988) Regulatory peptides in paraganglia. Prog Histochem Cytochem 18:1–92

    PubMed  CAS  Google Scholar 

  • Heym Ch, Lang R (1986) Transmitters in sympathetic postganglionic neurons. In: Panula P, Päivärinta H, Soinila S (eds) Neurohistochemistry — Modern methods and applications. Neurology and neurobiology, vol 16. Alan Liss, New York, pp 493–523

    Google Scholar 

  • Heym Ch, Reinecke M, Weihe E, Forssmann WG (1984) Dopamin-β-hydroxylase-, neurotensin-, substance P-, vasoactive intestinal polypeptide- and enkephalin-immunohistochemistry of paravertebral and prevertebral ganglia in the cat. Cell Tissue Res 235:411–418

    Article  PubMed  CAS  Google Scholar 

  • Hökfelt T, Elfvin L-G, Schultzberg M, Fuxe K, Said SI, Mutt V, Goldstein M (1977a) Immunohistochemical evidence of vasoactive intestinal polypeptide-containing neurons and nerve fibres in sympathetic ganglia. Neuroscience 2:885–896

    Article  Google Scholar 

  • Hökfelt T, Elfvin L-G, Schultzberg M, Goldstein M, Nilsson G (1977b) On the occurrence of substance P-containing fibres in sympathetic ganglia: immunohistochemical evidence. Brain Res 132:29–47

    Article  PubMed  Google Scholar 

  • Hökfelt T, Fuxe K, Goldstein M, Joh TH (1973) Immunohistochemical localization of three catecholamine synthesizing enzymes: aspects on methodology. Histochemie 33:231–254

    PubMed  Google Scholar 

  • Hohmann EL, Elde RP, Rysavy JA, Einzig S, Gebhard RL (1986) Innervation of periosteum and bone by sympathetic vasoactive intestinal peptide-containing nerve fibres. Science 232:868–871

    Article  PubMed  CAS  Google Scholar 

  • Inagaki S, Kito S (1986) Peptides in the peripheral nervous sytem. Progr Brain Res 66:269–316

    Article  CAS  Google Scholar 

  • Järhult J, Hellstrand P, Sundler F (1980) Immunohistochemical localization and vascular effects of vasoactive intestinal polypeptide in skeletal muscle of the cat. Cell Tissue Res 207:55–64

    Article  PubMed  Google Scholar 

  • Kessler JA, Adler JE, Bolen MC, Black IB (1981) Substance P in principal sympathetic neurons: regulation by impulse activity. Science 214:335–336

    Article  PubMed  CAS  Google Scholar 

  • Klein CM, Burden HW (1988) Substance P- and vasoactive intestinal polypeptide (VIP)-immunoreative nerve fibres in relation to ovarian postganglionic perikarya in para- and prevertebral ganglia: evidence from combined retrograde tracing and immunocytochemistry. Cell Tissue Res 252:403–410

    Article  PubMed  CAS  Google Scholar 

  • Krukoff TL, Ciriello J, Calaresu FR (1985) Segmental distribution of peptide-like immunoreactivity in cell bodies of the thoracolumbar sympathetic nuclei of the cat. J Comp Neurol 240:90–102

    Article  PubMed  CAS  Google Scholar 

  • Kummer W, Heym Ch (1986) Correlation of neuronal size and peptide immunoreactivity in the guinea-pig trigeminal ganglion. Cell Tissue Res 245:657–665

    Article  PubMed  CAS  Google Scholar 

  • Kummer W, Heym Ch (1988) Neuropeptide distribution in the cervico-thoracic paravertebral ganglia of the cat with particular reference to calcitonin gene-related peptide immunoreactivity. Cell Tissue Res 252:463–471

    Article  PubMed  CAS  Google Scholar 

  • Kummer W, Heym Ch, Colombo M, Lang R (1986) Immunohistochemical evidence for extrinsic and intrinsic opioid systems in the guinea pig superior cervical ganglion. Anat Embryol 174:401–405

    Article  PubMed  CAS  Google Scholar 

  • Kummer W, Reinecke M, Heym Ch, Forssmann W-G (1988) Distribution of opioid peptides functionally related to the cardiovascular system. In: Stumpe KO, Kraft E, Faden AI (eds) Opioid peptides and blood pressure control. Springer, Berlin Heidelberg New York, pp 5–12

    Google Scholar 

  • Landis SC, Fredieu JR (1986) Coexistence of calcitonin gene-related peptide and vasoactive intestinal peptide in cholinergic sympathtic innervation of sweat glands. Brain Res 377:177–181

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Takami K, Kawai Y, Girgis S, Hillyard CJ, MacIntyre I, Emson PC, Tohyama M (1985) Distribution of calcitonin gene-related peptide in the rat peripheral nervous system with reference to its coexistence with substance P. Neuroscience 15:1227–1237

    Article  PubMed  CAS  Google Scholar 

  • Lindh B, Hökfelt T, Elfvin L-G, Terenius L, Fahrenkrug J, Elde R, Goldstein M (1986) Topography of NPY-, somatostatin-, and VIP-immunoreactive, neuronal subpopulations in the guinea pig celiac-superior mesenteric ganglion and their projection to the pylorus. J Neurosci 6:2371–2383

    PubMed  CAS  Google Scholar 

  • Lindh B, Lundberg J, Hökfelt T, Elfvin LG, Fahrenkrug J, Fischer J (1987) Coexistence of CGRP- and VIP-like immunoreactivities in a population of neurons in the cat stellate ganglion. Acta Physiol Scand 131:475–476

    Article  PubMed  CAS  Google Scholar 

  • Lindh B, Lundberg J, Hökfelt T (1989) NPY-, galanin-, VIP/PHI-, CGRP- and substance P-immunoreactive neuronal subpopulations in cat autonomic and sensory ganglia and their projections. Cell Tissue Res 256:259–273

    Article  PubMed  CAS  Google Scholar 

  • Lundberg JM, Hökfelt T, Schultzberg M, Uvnäs-Wallenstein K, Köhler C, Said SI (1979) Occurrence of vasoactive intestinal polypeptide (VIP)-like immunoreactivity in certain cholinergic neurons of the cat: evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience 4:1539–1559

    Article  PubMed  CAS  Google Scholar 

  • Lundberg JM, Hökfelt T, Änggard A, Terenius L, Elde R, Markey K, Goldstein M (1982a) Organizational prinziples in the peripheral sympathetic nervous system: subdivision by coexisting peptides (somatostatin, avian pancreatic polypeptide and vasoactive intestinal polypeptide-like immunoreactivities). Proc Natl Acad Sci USA 79:1303–1307

    Article  PubMed  CAS  Google Scholar 

  • Lundberg JM, Terenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom S, Goldstein M (1982b) Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects of NPY on sympathic function. Acta Physiol Scand 116:477–480

    PubMed  CAS  Google Scholar 

  • Lundberg JM, Terenius L, Hökfelt T, Goldstein M (1983) High levels of neuropeptide Y in peripheral noradrenergic neurons in various mammals including man. Neurosci Lett 42:167–172

    Article  PubMed  CAS  Google Scholar 

  • Macrae IM, Furness JB, Costa M (1986) Distribution of subgroups of noradrenaline neurons in the coeliac ganglion of the guineapig. Cell Tissue Res 244:173–180

    Article  PubMed  CAS  Google Scholar 

  • Matsuyama T, Wanaka A, Kanagawa Y, Yoneda S, Kimura K, Hayakawa T, Kamada T, Tohyama M (1987) Two discrete enkephalinergic neuron systems in the superior cervical ganglion of the guinea pig: an immunoelectron microscopic study. Brain Res 418:325–333

    Article  PubMed  CAS  Google Scholar 

  • Matthews MR, Cuello AC (1982) Substance P-immunoreactive peripheral branches of sensory neurons innervate guinea pig sympathetic neurons. Proc Natl Acad Sci USA 79:1668–1672

    Article  PubMed  CAS  Google Scholar 

  • McLachlan EM, Llewellyn-Smith IJ (1986) The immunohistochemical distribution of neuropeptide Y in lumbar pre- and paravertebral sympathetic ganglia of the guinea pig. J Auton Nerv Syst 17:313–324

    Article  PubMed  CAS  Google Scholar 

  • Morris JL, Gibbins IL (1987) Neuronal colocalization of peptides, catecholamines, and catecholamine-synthesizing enzymes in guinea pig paracervical ganglia. J Neurosci 7:3117–3130

    PubMed  CAS  Google Scholar 

  • Morris JL, Gibbins IL, Furness JB, Costa M, Murphy R (1985) Co-localization of neuropeptide Y, vasoactive intestinal polypeptide and dynorphin in non-noradrenergic axons of the guinea pig uterine artery. Neurosci Lett 62:31–37

    Article  PubMed  CAS  Google Scholar 

  • Nielsch U, Keen P (1989) Reciprocal regulation of tachykinin- and vasoactive intestinal peptide-gene expression in rat sensory neurons following cut and crush injury. Brain Res 481:25–30

    Article  PubMed  CAS  Google Scholar 

  • Noon JP, McAffee DA, Roth RH (1975) Norepinephrine release from nerve terminals within the rabbit superior cervical ganglion. Naunyn Schmiedebergs Arch Pharmacol 291:139–162

    Article  PubMed  CAS  Google Scholar 

  • Schmitt M, Kummer W, Heym Ch (1988) Calcitonin gene-related peptide (CGRP)-immunoreactive neurons in the human cervico-thoracic paravertebral ganglia. J Chemical Neuroanat 1:287–292

    CAS  Google Scholar 

  • Schultzberg M, Hökfelt T, Terenius L, Elfvin L-G, Lundberg JM, Brandt J, Elde RP, Goldstein M (1979) Enkephalin immunoreactive nerve fibres and cell bodies in sympathetic ganglia of the guinea pig and rat. Neuroscience 4:249–270

    Article  PubMed  CAS  Google Scholar 

  • Senba E, Tohyama M (1988) Calcitonin gene-related peptide containing autonomic efferent pathways to the pelvic ganglia of the rat. Brain Res 449:386–390

    Article  PubMed  CAS  Google Scholar 

  • Shehab SAS, Atkinson ME (1986) Vasoactive intestinal polypeptide increases in the spinal cord after peripheral axotomy of the sciatic nerve originate from primary afferent neurons. Brain Res 372:37–44

    Article  PubMed  CAS  Google Scholar 

  • Vincent SR, Dalsgaard C-J, Schultzberg M, Hökfelt T, Christensson I, Terenius L (1984) Dynorphin-immunoreactive neurons in the autonomic nervous system. Neuroscience 11:973–981

    Article  PubMed  CAS  Google Scholar 

  • Webber R, Horn M, Heym Ch (1987) Peptide immunohistochemistry of guinea pig lumbar sympathetic ganglia. Exp Brain Res Series 16:34–38

    Google Scholar 

  • Webber R, Heym Ch (1988) Immunohistochemistry of biogenic polypeptides in nerve cells and fibres of the guinea pig inferior mesenteric ganglion after perturbations. Histochemistry 88:287–297

    PubMed  CAS  Google Scholar 

  • Weihe E, Hartschuh W, Weber E (1985a) Prodynorphin opioid peptides in small somatosensory primary afferents of guinea pig. Neurosci Lett 58:347–352

    Article  PubMed  CAS  Google Scholar 

  • Weihe E, McKnight AT, Corbett AD, Kosterlitz HW (1985b) Proenkephalin-and prodynorphin-derived opioid peptides in guinea pig heart. Neuropeptides 5:453–456

    Article  PubMed  CAS  Google Scholar 

  • Xiang JZ, Archelos J, Lang R (1984) Enkephalins in the heart. Clin Exp Theory Practice 6:1883–1888

    CAS  Google Scholar 

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Authors and Affiliations

  1. Institut für Anatomie und Zellbiologie der Universität Heidelberg, Im Neuenheimer Feld 307, D-6900, Heidelberg, FRG

    Ch. Heym, M. Horn & W. Kummer

  2. Department of Anatomical Sciences, Faculty of Health Sciences, State University of New York, 319 Farber Hall, 14214, Buffalo, NY, USA

    R. Webber

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  1. Ch. Heym
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  2. R. Webber
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  3. M. Horn
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  4. W. Kummer
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Heym, C., Webber, R., Horn, M. et al. Neuronal pathways in the guinea-pig lumbar sympathetic ganglia as revealed by immunohistochemistry. Histochemistry 93, 547–557 (1990). https://doi.org/10.1007/BF00266416

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