Skip to main content
Log in

Neuropeptide Y- and substance P-like immunoreactive nerve fibers in the rat dura mater encephali

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

Density and pattern of nerve fibers with neuropeptide Y-like immunoreactivity (NPY-LI) and substance P-like immunoreactivity (SP-LI) in the rat dura mater encephali were investigated by light and electron microscopy using whole-mount preparations. NPY-LI fibers are observed throughout the encephalic dura mater. A remarkable net of NPY-LI nerve fibers is located in the walls of the sagittal and transverse sinuses. Beyond that NPY-LI network, distinct NPY-LI nerve fibers or plexus occur in the rostral falx, parietal dura mater of the olfactory bulb, supratentorial dura mater, parietal dura mater of the cerebellum, tentorium cerebelli and the ventral dura mater. Electron microscopic studies reveal that NPY-LI is exclusively located in unmyelinated axons of small and large nerve fiber bundles, with or without a perineural sheath. Immunopositive C-fibers are predominantly associated with the vascular bed.

SP-LI nerve fibers have a moderate and more uniform distribution in the encephalic dura mater. A distinct plexus of SP-LI fibers follows the branches of the middle meningeal artery and the adjacent dura mater. SP-LI fibers are most prominent in the parietal dura mater of the cerebellum. Fine beaded SP-LI fibers, arising from larger SP-LI fiber bundles, are observed in close association to the capillary bed. SP-LI axons are all unmyelinated. They are found in larger nerve fiber bundles with a perineural sheath or in Schwann cells lacking any perineural sheath.

The function of NPY-LI and SP-LI nerve fibers in the rat dura mater is discussed in relation to their topography, density and termination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amenta F, Sancesario G, Ferrante F, Cavallotti C (1980) Acetylcholinesterase-containing nerve fibers in the dura mater of guinea pig, mouse and rat. J Neural Transm 47:237–242

    Article  PubMed  CAS  Google Scholar 

  • Andres KH, v Düring M, Muszynski K, Schmidt RF (1987a) Nerve fibers and their terminals of the dura mater encephali of the rat. Anat Embryol 175:289–301

    Article  PubMed  CAS  Google Scholar 

  • Andres KH, v Düring M, Muszynski K, Schmidt RF (1987b) The innervation of the dura mater encephali of the rat. In: Schmidt RF, Schaible HG, Vahle-Hinz C (eds) Fine afferent nerve fibers and pain. VHC Verlagsgesellschaft mbH Weinheim, pp 17–25

  • Edvinsson L, Uddman R (1981) Adrenergic, cholinergic and peptidergic nerve fibers in dura mater — involvement in headache? Cephalalgia 1:175–179

    Article  PubMed  CAS  Google Scholar 

  • Edvinsson L, Rosendal-Helgesen S, Uddman R (1983a) Substance P: Localization, concentration and release in cerebral arteries, choroid plexus and dura mater. Cell Tissue Res 234:1–7

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Edvinsson L, Copeland JR, Emson PC, McCulloch J, Uddman R (1987) Nerve fibers containing neuropeptide Y in the cerebrovascular bed: immunocytochemistry, radioimmunoassay and vasomotor effects. J Cereb Blood Flow Metab 7:45–57

    PubMed  CAS  Google Scholar 

  • Edvinsson L, Brodin E, Jansen I, Uddman R (1988) Neurokinin A in cerebral vessels: characterization, localization and effects in vitro. Regul Pept 20:181–197

    Article  PubMed  CAS  Google Scholar 

  • Ekblad E, Edvinsson L, Wahlestedt C, Uddman R, Håkanson R, Sundler F (1984) Neuropeptide Y co-exists and co-operates with noradrenaline in perivascular nerve fibers. Regul Pept 8:225–235

    Article  PubMed  CAS  Google Scholar 

  • Furness JB, Papka RE, Della NG, Costa M, Eskay RL (1982) Substance P-like immunoreactivity in nerves associated with the vascular system of guinea-pigs. Neuroscience 7:447–459

    Article  PubMed  CAS  Google Scholar 

  • Gibbins IL, Morris JL (1988) Co-existence of immunoreactivity to neuropeptide Y and vasoactive intestinal peptide in nonnoradrenergic axons innervating guinea pig cerebral arteries after sympathectomy. Brain Res 444:402–406

    Article  PubMed  CAS  Google Scholar 

  • Iwanaga T, Fujita T, Yanaihara N (1985) Nerve fibers in the urethral mucosa of canine penis are immunoreactive for both substance P and calcitonin gene-related peptide. Arch Histol Jpn 48:547–554

    PubMed  CAS  Google Scholar 

  • Jancso N, Jancso-Gabor A, Szolcsanyi J (1967) Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br J Pharmacol Chemother 31:138–151

    PubMed  CAS  Google Scholar 

  • Keller JT, Saunders MC, Beduk A, Jollis JG (1985) Innervation of the posterior fossa dura of the cat. Brain Res Bull 14:97–102

    Article  PubMed  CAS  Google Scholar 

  • Keller JT, Marfurt CF, Dimlich RVW, Tierney BE (1989) Sympathetic innervation of the supratentorial dura mater of the rat. J Comp Neurol 290:310–321

    Article  PubMed  CAS  Google Scholar 

  • Kimmel DL (1961) Innervation of spinal dura mater and dura mater of the posterior cranial fossa. Neurology 11:800–809

    PubMed  CAS  Google Scholar 

  • Leblanc GG, Trimmer BA, Landis SC (1987) Neuropeptide Y-like immunoreactivity in rat cranial parasympathetic neurons: Coexistence with vasoactive intestinal peptide and choline acetyl transferase. Proc Natl Acad Sci USA 84:3511–3515

    Article  PubMed  CAS  Google Scholar 

  • Lembeck F (1985) Substance P and sensory neurones. In: Jordan CC, Oehme P (eds) Substance P. metabolism and biological actions, Taylor & Francis, London, pp 137–151

    Google Scholar 

  • Lembeck F, Holzer P (1979) Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn-Schmiedebergs Arch Pharmacol 310:175–183

    Article  PubMed  CAS  Google Scholar 

  • Lembeck F, Donnerer J, Barthó L (1982) Inhibition of neur ogenic vasodilatation and plasma extravasation by substance P antagonists, somatostatin and (d-meth2, pro5) enkephalinamide. Eur J Pharmacol 85:171–176

    Article  PubMed  CAS  Google Scholar 

  • McDonald DM (1988) Neurogenic inflammation in the rat trachea. I. Changes in venules, leucocytes and epithelial cells. J Neurocytol 17:583–603

    Article  PubMed  CAS  Google Scholar 

  • Markowitz S, Saito K, Moskowitz MA (1987) Neurogenically mediated leakage of plasma protein occurs from blood vessels in dura mater but not brain. J Neurosci 7:4129–4136

    PubMed  CAS  Google Scholar 

  • Mayberg M, Langer RS, Zervas NT, Moskowitz MA (1981) Perivascular meningeal projections from cat trigeminal ganglia: Possible pathway for vascular headaches in man. Science 213:228–230

    PubMed  CAS  Google Scholar 

  • Mayberg M, Zervas NT, Moskowitz MA (1984) Trigeminal projections to supratentorial pial and dural blood vessels in cats demonstrated by horseradish peroxidase histochemistry. J Comp Neurol 233:46–56

    Article  Google Scholar 

  • Moskowitz M, Liu-Chen LY, Mayberg MR, Zervas NT, Han DH, Brody MR (1983) Cat pio-arachnoid contains immunoreactive substance P within neurons projecting from the fifth cranial nerve. In: Reivich M, Hurtig HI (eds) Cereb Dis 363–371 Raven Press, New York

    Google Scholar 

  • Moskowitz MY (1984) The neurobiology of vascular head pain. Ann Neurol 16:157–168

    Article  PubMed  CAS  Google Scholar 

  • Moskowitz MY, Buzzi MG, Sakas DE, Linnik ME (1989) Pain mechanisms underlying vascular headaches. Rev Neurol (Paris) 145:181–193

    CAS  Google Scholar 

  • O’Connor TP, van der Kooy D (1986) Pattern of intracranial and extracranial projections of trigeminal ganglion cells. J Neurosci 6:2200–2207

    PubMed  CAS  Google Scholar 

  • Penfield W, McNaughton F (1940) Dural headache and innervation of the dura mater. Arch Neurol Psychiatry 44:43–75

    Google Scholar 

  • Pernow B (1983) Substance P. Pharmacol Rev 35:85–141

    PubMed  CAS  Google Scholar 

  • Ray BS, Wolff HG (1940) Experimental studies on headache. Pain sensitive structures of the head and their significance in headache. Arch Surg 41:813–856

    Google Scholar 

  • Silverman J, Kruger L (1989) Calcitonin-gene-related-peptide-immunoreactive innervation of the rat head with emphasis on specialized sensory structures. J Comp Neurol 280:303–330

    Article  PubMed  CAS  Google Scholar 

  • Steiger HJ, Tew JM, Keller JT (1982) The sensory representation of the trigeminal ganglion of the cat. Neurosci Lett 31:231–236

    Article  PubMed  CAS  Google Scholar 

  • Suzuki N, Hardebo JE, Owman Ch (1988) Origin and pathways of cerebrovascular vasoactie intestinal polypeptide-positive nerves in rat. J Cereb Blood Flow Metab 8:697–712

    PubMed  CAS  Google Scholar 

  • Suzuki N, Hardebo JE, Owman Ch (1989a) Origins and pathways of cerebrovascular nerves storing substance P and calcitonin gene-related peptide in rat. Neuroscience 2:427–438

    Article  Google Scholar 

  • Suzuki N, Hardebo JE, Kahrström J, Owman Ch (1989b) Neuropeptide Y coexists with vasoactive intestinal polypeptide in parasympathetic cerebrovascular nerves originating in the sphenopalatine, otic and internal carotid ganglia of the rat. Neurscience (submitted)

  • Uddman R, Edvinsson L, Ekman R, Kingman R, McCulloch J (1985) Innervation of the feline cerebral vasculature by nerve fibers containing calcitonin-related peptide: trigeminal origin and co-existence with substance P. Neurosci Lett 62:131–136

    Article  PubMed  CAS  Google Scholar 

  • Uddman R, Hara H, Edvinsson L (1989) Neuronal pathways to the rat middle meningeal artery revealed by retrograde tracing and immunocytochemistry. J Auton Nerv Syst 26:69–75

    Article  PubMed  CAS  Google Scholar 

  • Wirth FP, Van Buren JM (1971) Referral of pain from dural stimulation in man. J Neurosurg 34:630–642

    Article  PubMed  Google Scholar 

  • Yamamoto K, Matsuyama T, Shiosaka S, Inagaki S, Senba E, Shimizu Y, Ishimoto I, Hayakawa T, Matsumoto M, Tohyama M (1983) Overall distribution of substance P-containing nerves in the wall of the cerebral arteries of the guinea-pig and its origin. J Comp Neurol 215:421–426

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

von Düring, M., Bauersachs, M., Böhmer, B. et al. Neuropeptide Y- and substance P-like immunoreactive nerve fibers in the rat dura mater encephali. Anat Embryol 182, 363–373 (1990). https://doi.org/10.1007/BF02433496

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02433496

Key words

Navigation