Neonatal Damage to the Rat's Infraorbital Nerve Upregulates Both Galanin and Neuropeptide Y in Individual Vibrissae-related Primary Afferent Axons

Overview

Journal Exp Brain Res

Specialty Neurology

Date 1996 Dec 1

PMID 9007549

Authors

C B Boylan

K Davis

C A Bennett-Clarke

R W Rhoades

Affiliations

Soon will be listed here.

Abstract

Previous studies in adult animals have suggested that the peptides galanin and neuropeptide Y (NPY) may be upregulated in the same primary afferent neurons after peripheral axotomy. The present study was undertaken to determine whether such upregulation occurred in vibrissae-related primary afferent neurons and their axons after damage to the infraorbital nerve [ION; the trigeminal (V) branch that innervates the vibrissae follicles]. Double-labelling experiments demonstrated that approximately 75% of axotomized V ganglion cells and the central arbors of vibrissae-related primary afferents expressed both galanin and NPY after perinatal, but not adult, nerve damage. However, additional experiments demonstrated that the sensitive periods for lesion-induced upregulation of the two peptides and the period over which they were expressed after neonatal ION transection differed substantially. Staining for both peptides was increased after ION damage on P-0 through P-14, but only galanin staining was increased in vibrissae-related primary afferents after lesions on P-21. Galanin expression was elevated in vibrissae-related primary afferents in rats killed 3, 8, and 15 days after neonatal ION transection, while increased NPY was observed at only the middle time point. The lesion-induced increases in galanin and NPY in vibrissae-related ION primary afferents suggest that these peptides may modulate central V reorganization after such damage.

References

Ju G, Hokfelt T, Brodin E, Fahrenkrug J, Fischer J, Frey P . 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. 1987; 247(2):417-31. DOI: 10.1007/BF00218323. View

Colmers W, Bleakman D . Effects of neuropeptide Y on the electrical properties of neurons. Trends Neurosci. 1994; 17(9):373-9. DOI: 10.1016/0166-2236(94)90046-9. View

Chiaia N, Fish S, Bauer W, Figley B, Eck M, Bennett-Clarke C . Effects of postnatal blockade of cortical activity with tetrodotoxin upon the development and plasticity of vibrissa-related patterns in the somatosensory cortex of hamsters. Somatosens Mot Res. 1994; 11(3):219-28. DOI: 10.3109/08990229409051390. View

Wiesenfeld-Hallin Z, Villar M, Hokfelt T . The effects of intrathecal galanin and C-fiber stimulation on the flexor reflex in the rat. Brain Res. 1989; 486(2):205-13. DOI: 10.1016/0006-8993(89)90506-4. View

Toth P, Bindokas V, Bleakman D, Colmers W, Miller R . Mechanism of presynaptic inhibition by neuropeptide Y at sympathetic nerve terminals. Nature. 1993; 364(6438):635-9. DOI: 10.1038/364635a0. View

Kuraishi Y, Minami M, Satoh M . Serotonin, but neither noradrenaline nor GABA, inhibits capsaicin-evoked release of immunoreactive somatostatin from slices of rat spinal cord. Neurosci Res. 1991; 9(4):238-45. DOI: 10.1016/0168-0102(91)90025-t. View

Villar M, Wiesenfeld-Hallin Z, Xu X, Theodorsson E, Emson P, Hokfelt T . Further studies on galanin-, substance P-, and CGRP-like immunoreactivities in primary sensory neurons and spinal cord: effects of dorsal rhizotomies and sciatic nerve lesions. Exp Neurol. 1991; 112(1):29-39. DOI: 10.1016/0014-4886(91)90111-o. View

Wiesenfeld-Hallin Z, Xu X, Hakanson R, Feng D, Folkers K, Kristensson K . On the role of substance P, galanin, vasoactive intestinal peptide, and calcitonin gene-related peptide in mediation of spinal reflex excitability in rats with intact and sectioned peripheral nerves. Ann N Y Acad Sci. 1991; 632:198-211. DOI: 10.1111/j.1749-6632.1991.tb33108.x. View

Hayashi H . Distributions of vibrissae afferent fiber collaterals in the trigeminal nuclei as revealed by intra-axonal injection of horseradish peroxidase. Brain Res. 1980; 183(2):442-6. DOI: 10.1016/0006-8993(80)90478-3. View

10.

Jacquin M, Stennett R, Renehan W, Rhoades R . Structure-function relationships in the rat brainstem subnucleus interpolaris: II. Low and high threshold trigeminal primary afferents. J Comp Neurol. 1988; 267(1):107-30. DOI: 10.1002/cne.902670108. View

11.

Colmers W, Lukowiak K, Pittman Q . Presynaptic action of neuropeptide Y in area CA1 of the rat hippocampal slice. J Physiol. 1987; 383:285-99. PMC: 1183070. DOI: 10.1113/jphysiol.1987.sp016409. View

12.

Wakisaka S, Takikita S, Sasaki Y, Kato J, Tabata M, Kurisu K . Cell size-specific appearance of neuropeptide Y in the trigeminal ganglion following peripheral axotomy of different branches of the mandibular nerve of the rat. Brain Res. 1993; 620(2):347-50. DOI: 10.1016/0006-8993(93)90179-q. View

13.

Yanagisawa M, Yagi N, Otsuka M, Yanaihara C, Yanaihara N . Inhibitory effects of galanin on the isolated spinal cord of the newborn rat. Neurosci Lett. 1986; 70(2):278-82. DOI: 10.1016/0304-3940(86)90477-5. View

14.

White F, Chiaia N, McCann P, Enfiejian H, Macdonald G, Bennett-Clarke C . Selective sparing of later-born ganglion cells after neonatal transection of the infraorbital nerve. J Comp Neurol. 1993; 331(2):236-44. DOI: 10.1002/cne.903310207. View

15.

Schlaggar B, Fox K, OLeary D . Postsynaptic control of plasticity in developing somatosensory cortex. Nature. 1993; 364(6438):623-6. DOI: 10.1038/364623a0. View

16.

Hokfelt T, Wiesenfeld-Hallin Z, Villar M, Melander T . Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci Lett. 1987; 83(3):217-20. DOI: 10.1016/0304-3940(87)90088-7. View

17.

Henderson T, Woolsey T, Jacquin M . Infraorbital nerve blockade from birth does not disrupt central trigeminal pattern formation in the rat. Brain Res Dev Brain Res. 1992; 66(1):146-52. DOI: 10.1016/0165-3806(92)90152-m. View

18.

Verge V, Richardson P, Wiesenfeld-Hallin Z, Hokfelt T . Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. J Neurosci. 1995; 15(3 Pt 1):2081-96. PMC: 6578124. View

19.

Kombian S, Colmers W . Neuropeptide Y selectively inhibits slow synaptic potentials in rat dorsal raphe nucleus in vitro by a presynaptic action. J Neurosci. 1992; 12(3):1086-93. PMC: 6576054. View

20.

Ju G, Melander T, Ceccatelli S, Hokfelt T, Frey P . Immunohistochemical evidence for a spinothalamic pathway co-containing cholecystokinin- and galanin-like immunoreactivities in the rat. Neuroscience. 1987; 20(2):439-56. DOI: 10.1016/0306-4522(87)90103-5. View