Skip to main content
Log in

Calcitonin gene-related peptide-immunoreactivity in functionally identified primary afferent neurones in the rat

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

In anaesthetized rats, intracellular recordings were made from the somata of lumbar (L4 and L5) dorsal root ganglion cells. The impaled afferent units were first functionally classified by testing the peripheral receptive endings with mechanical stimuli and then iontophoretically injected with a fluorescent dye. Serial sections of the dorsal root ganglion containing the injected soma were incubated with an antibody solution against calcitonin gene-related peptide (CGRP). Somata displaying calcitonin gene-related peptide-immunoreactivity (CGRP-IR) possessed receptive endings in the skin and deep somatic tissues (muscle, fascia, tendon, joint). The majority of calcitonin gene-related peptide-immunoreactive (CGRP-ir) neurones had conduction velocities below 2.5 m/s; only a few neurones conducted faster than 10 m/s. The immunostained somata were small to mediumsized (cross-sectional area < 1200 μm2). With one exeption, CGRP-IR was found in all types of ending studied, but the proportion of CGRP-ir neurones differed. Immunostained somata were rare among cutaneous and deep low-threshold mechanosensitive units (e.g. hair follicle and muscle spindle units). CGRP-ir somata were most frequent among high-threshold mechanosensitive (presumably nociceptive) afferent neurones (four out of six cells). The data suggest that CGRP can be expressed not only in nociceptive but also in many other types of primary afferent neurone, the condition being that the conduction velocity is slow and/or the cell soma small.

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.

Similar content being viewed by others

References

  • Carr PA, Yamamoto T, Nagy JI (1990) Calcitonin gene-related peptide in primary afferent neurons of rat: co-existence with fluoride-resistant acid phosphatase and depletion by neonatal capsaicin. Neuroscience 36:751–760

    Google Scholar 

  • Chung K, Lee WT, Carlton SM (1988) The effects of dorsal cord isolation on calcitonin gene-related peptide-labeled terminals in the rat lumbar dorsal horn. Neurosci Lett 90:27–32

    Google Scholar 

  • Forssmann W-G, Pickel V, Reinecke M, Hock D, Metz J (1981) Immunochemistry and immunocytochemistry of nervous tissue. In: Heym CH, Forssman W-G (eds) Techniques in neuroanatomical research. Springer, Berlin Heidelberg New York, pp 171–205

    Google Scholar 

  • Gibson SJ, Polak JM, Bloom SR, Sabate IM, Mulderry PM, Ghatei MA, McGregor GP, Morrison JFB, Kelly JS, Evans RM, Rosenfeld MG (1984) Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J Neurosci 4:3101–3111

    Google Scholar 

  • Hanesch U, Heppelmann B, Schmidt RF (1991) Substance P- and calcitonin gene-related peptide immunoreactivity in primary afferent neurons of the cat's knee joint. Neuroscience 45:185–193

    Google Scholar 

  • Harper AA, Lawson SN (1985a) Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol 359:31–46

    Google Scholar 

  • Harper AA, Lawson SN (1985b) Electrical properties of rat dorsal root ganglion neurones with different peripheral nerve conduction velocities. J Physiol 359:47–63

    Google Scholar 

  • Hayes CE, Goldstein IJ (1974) A α-d-galactosyl-binding lectin from Bandeiraea simplicifolia seeds. J Biol Chem 249:1904–1914

    Google Scholar 

  • Hoheisel U, Mense S (1987) Observations on the morphology of axons and somata of slowly conducting dorsal root ganglion cells in the cat. Brain Res 423:269–278

    Google Scholar 

  • Hoheisel U, Lehmann-Willenbrock E, Mense S (1989) Termination patterns of identified group II and III afferent fibres from deep tissues in the spinal cord of the cat. Neuroscience 28:495–507

    Google Scholar 

  • Hunt CC (1990) Mammalian muscle spindle: peripheral mechanisms. Physiol Rev 70:643–663

    Google Scholar 

  • Hunt SP, Rossi J (1985) Peptide- and non-peptide-containing unmyelinated primary afferents: the parallel processing of nociceptive information. Philos Trans R Soc Lond [Biol] 308:283–289

    Google Scholar 

  • Ishida-Yamamoto A, Tohyama M (1989) Calcitonin gene-related peptide in the nervous tissue. Prog Neurobiol 33:335–386

    Google Scholar 

  • Ju G, Hökfelt T, Brodin E, Fahrenkrug J, Fischer AJ, Frey P, Elde RP, Brown JC (1987) Primary sensory neurons of the rat showing calcitonin gene-related peptide immunoreactivity and their relation to substance P-, somatostatin-, galanin-, vasoactive intestinal polypeptide- and cholecystokinin-immunoreactive ganglion cells. Cell Tissue Res 247:417–431

    Google Scholar 

  • Kakudo K, Hasegawa H, Komatsu N, Nakamura A, Itoh Y, Watanabe K (1988) Immuno-electron microscopic study of calcitonin gene-related peptide (CGRP) in axis cylinders of the vagus nerve. CGRP is present in both myelinated and unmyelinated fibers. Brain Res 440:153–158

    Google Scholar 

  • Kow LM, Pfaff DW (1979) Responses of single units in sixth lumbar dorsal root ganglion of female rats to mechanostimulation relevant for lordosis reflex. J Neurophysiol 42:203–213

    Google Scholar 

  • Kruger L, Silverman JD, Manthy PW, Sternini C, Brecha NC (1989) Peripheral patterns of calcitonin gene-related peptide general somatic sensory innervation: cutaneous and deep terminations. J Comp Neurol 280:291–302

    Google Scholar 

  • Kuraishi Y, Nanayama T, Ohno H, Minami M, Satoh M (1988) Antinociception induced in rats by intrathecal administration of antiserum against calcitonin gene-related peptide. Neurosci Lett 92:325–329

    Google Scholar 

  • Leah JD, Cameron AA, Snow PJ (1985) Neuropeptides in physiologically identified mammalian sensory neurones. Neurosci Lett 56:257–263

    Google Scholar 

  • Lee KH, Chung K, Chung MJ, Coggeshall RE (1986) Correlation of cell body size, axon size, and signal conduction velocity for individually labelled dorsal root ganglion cells in the cat. J Comp Neurol 243:335–346

    Google Scholar 

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

    Google Scholar 

  • Light AR, Perl ER (1979) Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 186:133–150

    Google Scholar 

  • Lynn B, Carpenter SE (1982) Primary afferent units from the hairy skin of the rat hind limb. Brain Res 238:29–43

    Google Scholar 

  • Marx JL (1979) Brain peptides: is substance P a transmitter of pain signals? Science 205:886–889

    Google Scholar 

  • McCarthy PW, Lawson SN (1989) Cell type and conduction velocity of rat primary sensory neurons with substance P-like immunoreactivity. Neuroscience 28:745–753

    Google Scholar 

  • McCarthy PW, Lawson SN (1990) Cell type and conduction velocity of rat primary sensory neurons with calcitonin gene-related peptide-like immunoreactivity. Neuroscience 34:623–632

    Google Scholar 

  • Molander C, Ygge J, 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

    Google Scholar 

  • Morton CR, Hutchison WD (1989) Release of sensory neuropeptides in the spinal cord: studies with calcitonin gene-related peptide and galanin. Neuroscience 31:807–815

    Google Scholar 

  • O'Brien C, Woolf CJ, Fitzgerald M, Lindsay RM, Molander C (1989) Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint. Neuroscience 32:493–502

    Google Scholar 

  • Otsukai M, Yanagissawa M (1987) Does substance P act as a pain transmitter? Trends Pharmacol Sci 8:501–505

    Google Scholar 

  • Plenderleith MB, Cameron AA, Key B, Snow PJ (1989) The plant lectin soybean agglutinin binds to the soma, axon and central terminals of a subpopulation of small-diameter primary sensory neurons in the rat and cat. Neuroscience 31:683–695

    Google Scholar 

  • Ryu PD, Gerber G, Murase K, Randic M (1988) Actions of calcitonin gene-related peptide on rat spinal dorsal horn neurons. Brain Res 441:357–361

    Google Scholar 

  • Scharfman HE, Kunkel DD, Schwartzkroin PA (1989) Intracellular dyes mask immunoreactivity of hippocampal interneurons. Neurosci Lett 96:23–28

    Google Scholar 

  • Silverman JD, Kruger L (1988) Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated “nociceptor” thin axons in rat testis and cornea whole-mount preparations. Somatosens Res 5:259–267

    Google Scholar 

  • Stoward PJ, Spicer SS, Miller RL (1980) Histochemical reactivity for peanut lectin-horseradish peroxidase conjugate. J Histochem Cytochem 28:979–990

    Google Scholar 

  • Streit WJ, Schulte BA, Balentine JD, Spicer SS (1986) Evidence for glycoconjugate in nociceptive primary sensory neurons and its origin from the Golgi complex. Brain Res 377:1–17

    Google Scholar 

  • Woolf CJ, Wiesenfeld-Hallin Z (1986) Substance P and calcitonin gene-related peptide synergistically modulate the gain of the nociceptive flexor withdrawal reflex in the rat. Neurosci Lett 66:226–230

    Google Scholar 

  • Yoshida S, Matsuda Y (1979) Studies on sensory neurons of the mouse with intracellular-recording and horseradish peroxidase-injection techniques. J Neurophysiol 42:1134–1145

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoheisel, U., Mense, S. & Scherotzke, R. Calcitonin gene-related peptide-immunoreactivity in functionally identified primary afferent neurones in the rat. Anat Embryol 189, 41–49 (1994). https://doi.org/10.1007/BF00193128

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00193128

Key words

Navigation