Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Journal of Neuroinflammation
Published in: Journal of Neuroinflammation 1/2011

Open Access 01-12-2011 | Research

Differential contribution of electrically evoked dorsal root reflexes to peripheral vasodilatation and plasma extravasation

Authors: Oleg V Lobanov, Yuan B Peng

Published in: Journal of Neuroinflammation | Issue 1/2011

Login to get access

Abstract

Background

Dorsal root reflexes (DRRs) are antidromic activities traveling along the primary afferent fibers, which can be generated by peripheral stimulation or central stimulation. DRRs are thought to be involved in the generation of neurogenic inflammation, as indicated by plasma extravasation and vasodilatation. The hypothesis of this study was that electrical stimulation of the central stump of a cut dorsal root would lead to generation of DRRs, resulting in plasma extravasation and vasodilatation.

Methods

Sprague-Dawley rats were prepared to expose spinal cord and L4-L6 dorsal roots under pentobarbital general anesthesia. Electrical stimulation of either intact, proximal or distal, cut dorsal roots was applied while plasma extravasation or blood perfusion of the hindpaw was recorded.

Results

While stimulation of the peripheral stump of a dorsal root elicited plasma extravasation, electrical stimulation of the central stump of a cut dorsal root generated significant DRRs, but failed to induce plasma extravasation. However, stimulation of the central stump induced a significant increase in blood perfusion.

Conclusions

It is suggested that DRRs are involved in vasodilatation but not plasma extravasation in neurogenic inflammation in normal animals.
Appendix
Available only for authorised users
Literature
1.
Gotch F, Horsley V: On the mammalian nervous system, its functions and their localizations, determined by an electrical method. Philosophical transactions of the Royal Society of London Series B, Biological sciences. 1891, 276-526.
2.
3.
4.
Barron DH, Matthews BHC: Dorsal root potentials. Journal of Physiology. 1938, 94: 27-28P.
5.
Barron DH, Matthews BHC: Dorsal root reflexes. Journal of Physiology. 1938, 94: 26-27P.CrossRef
6.
7.
Langford LA, Coggeshall RE: Branching of sensory axons in the dorsal root and evidence for the absence of dorsal root efferent fibers. The Journal of comparative neurology. 1979, 184: 193-204. 10.1002/cne.901840111.CrossRefPubMed
8.
Brooks CM, Koizumi K: Origin of the dorsal root reflex. Journal of Neurophysiology. 1956, 19: 60-74.PubMed
9.
Brooks CM, Koizumi K, Malcolm JL: Effects of changes in temperature on reactions of spinal cord. Journal of Neurophysiology. 1955, 18: 205-216.PubMed
10.
Iwamoto I, Nadel JA: Tachykinin receptor subtype that mediates the increase in vascular permeability in guinea pig skin. Life Science. 1989, 44: 1089-1095. 10.1016/0024-3205(89)90336-6.CrossRef
11.
Brain SD: Sensory neuropeptides: their role in inflammation and wound healing. Immunopharmacology. 1997, 37: 133-152. 10.1016/S0162-3109(97)00055-6.CrossRefPubMed
12.
Majno G, Shea SM, Leventhal M: Endothelial contraction induced by histamine-type mediators: an electron microscopic study. The Journal of cell biology. 1969, 42: 647-672. 10.1083/jcb.42.3.647.PubMedCentralCrossRefPubMed
13.
Holzer P: Neurogenic vasodilatation and plasma leakage in the skin. General Pharmacology. 1998, 30: 5-11.CrossRefPubMed
14.
Harrison S, Geppetti P: Substance p. The international journal of biochemistry & cell biology. 2001, 33: 555-576.CrossRef
15.
Brain SD, Cambridge H: Calcitonin gene-related peptide: vasoactive effects and potential therapeutic role. General Pharmacology. 1996, 27: 607-611.CrossRefPubMed
16.
Levine JD, Clark R, Devor M, Helms C, Moskowitz MA, Basbaum AI: Intraneuronal substance P contributes to the severity of experimental arthritis. Science. 1984, 226: 547-549. 10.1126/science.6208609.CrossRefPubMed
17.
Lundberg JM, Franco-Cereceda A, Hua X, Hökfelt T, Fischer JA: Co-existence of substance P and calcitonin gene-related peptide-like immunoreactivities in sensory nerves in relation to cardiovascular and bronchoconstrictor effects of capsaicin. European Journal of Pharmacology. 1985, 108: 315-319. 10.1016/0014-2999(85)90456-X.CrossRefPubMed
18.
Maggi CA, Meli A: The sensory-efferent function of capsaicin-sensitive sensory neurons. General Pharmacology. 1988, 19: 1-43.CrossRefPubMed
19.
Holzer P: Peptidergic sensory neurons in the control of vascular functions: mechanisms and significance in the cutaneous and splanchnic vascular beds. Reviews of physiology, biochemistry and pharmacology. 1992, 121: 49-146. full_text.PubMed
20.
Szolcsányi J: Antidromic vasodilatation and neurogenic inflammation. Agents Actions. 1988, 23: 4-11.CrossRefPubMed
21.
Pinter E, Szolcsányi J: Inflammatory and antiinflammatory effects of antidromic stimulation of dorsal roots in the rat. Agents Actions. 1988, 25: 240-242. 10.1007/BF01965023.CrossRefPubMed
22.
Gee MD, Lynn B, Cotsell B: The relationship between cutaneous C fibre type and antidromic vasodilatation in the rabbit and the rat. Journal of Physiology. 1997, 503: 31-44. 10.1111/j.1469-7793.1997.031bi.x.PubMedCentralCrossRefPubMed
23.
Ferrell WR, Russell NJ: Extravasation in the knee induced by antidromic stimulation of articular C fibre afferents of the anaesthetized cat. Journal of Physiology. 1986, 379: 407-416.PubMedCentralCrossRefPubMed
24.
Jänig W, Lisney SJ: Small diameter myelinated afferents produce vasodilatation but not plasma extravasation in rat skin. Journal of Physiology. 1989, 415: 477-486.PubMedCentralCrossRefPubMed
25.
Kenins P: Identification of the unmyelinated sensory nerves which evoke plasma extravasation in response to antidromic stimulation. Neuroscience Letters. 1981, 25: 137-141. 10.1016/0304-3940(81)90321-9.CrossRefPubMed
26.
Takahashi Y, Nakajima Y: Dermatomes in the rat limbs as determined by antidromic stimulation of sensory C-fibers in spinal nerves. Pain. 1996, 67: 197-202. 10.1016/0304-3959(96)03116-8.CrossRefPubMed
27.
Lin Q, Wu J, Willis WD: Dorsal root reflexes and cutaneous neurogenic inflammation after intradermal injection of capsaicin in rats. Journal of Neurophysiology. 1999, 82: 2602-2611.PubMed
28.
Rees H, Sluka KA, Westlund KN, Willis WD: Do dorsal root reflexes augment peripheral inflammation?. Neuroreport. 1994, 5: 821-824. 10.1097/00001756-199403000-00021.CrossRefPubMed
29.
Rees H, Sluka KA, Westlund KN, Willis WD: The role of glutamate and GABA receptors in the generation of dorsal root reflexes by acute arthritis in the anaesthetized rat. Journal of Physiology. 1995, 484 (Pt 2): 437-445.PubMedCentralCrossRefPubMed
30.
Sluka KA, Westlund KN: Centrally administered non-NMDA but not NMDA receptor antagonists block peripheral knee joint inflammation. Pain. 1993, 55: 217-225. 10.1016/0304-3959(93)90150-N.CrossRefPubMed
31.
Sluka KA, Lawand NB, Westlund KN: Joint inflammation is reduced by dorsal rhizotomy and not by sympathectomy or spinal cord transection. Annals of the rheumatic diseases. 1994, 53: 309-314. 10.1136/ard.53.5.309.PubMedCentralCrossRefPubMed
32.
Rees H, Sluka KA, Lu Y, Westlund KN, Willis WD: Dorsal root reflexes in articular afferents occur bilaterally in a chronic model of arthritis in rats. Journal of Neurophysiology. 1996, 76: 4190-4193.PubMed
33.
Hayes ES, Carlton SM: Primary afferent interactions: analysis of calcitonin gene-related peptide-immunoreactive terminals in contact with unlabeled and GABA-immunoreactive profiles in the monkey dorsal horn. Neuroscience. 1992, 47: 873-896. 10.1016/0306-4522(92)90037-3.CrossRefPubMed
34.
Sluka KA, Willis WD, Westlund KN: The Role of Dorsal Root Reflexes in Neurogenic Inflammation. Pain Forum. 1995, 4 (3): 141-149.CrossRef
35.
Zou X, Lin Q, Willis WD: NMDA or non-NMDA receptor antagonists attenuate increased Fos expression in spinal dorsal horn GABAergic neurons after intradermal injection of capsaicin in rats. Neuroscience. 2001, 106: 171-182. 10.1016/S0306-4522(01)00175-0.CrossRefPubMed
36.
Zou X, Lin Q, Willis WD: The effects of sympathectomy on capsaicin-evoked fos expression of spinal dorsal horn GABAergic neurons. Brain Research. 2002, 958: 322-329. 10.1016/S0006-8993(02)03621-1.CrossRefPubMed
37.
Curtis DR, Lodge D: The depolarization of feline ventral horn group Ia spinal afferent terminations by GABA. Experimental Brain Research. 1982, 46: 215-233. 10.1007/BF00237180.CrossRefPubMed
38.
Levy RA: GABA: a direct depolarizing action at the mammalian primary afferent terminal. Brain Research. 1974, 76: 155-160. 10.1016/0006-8993(74)90522-8.CrossRefPubMed
39.
Schmidt RF: Presynaptic inhibition in the vertebrate central nervous system. Ergeb Physiol. 1971, 63: 20-101. full_text.PubMed
40.
Willis WD: Dorsal root potentials and dorsal root reflexes: a double-edged sword. Experimental Brain Research. 1999, 124: 395-421. 10.1007/s002210050637.CrossRefPubMed
41.
Sluka KA, Rees H, Westlund KN, Willis WD: Fiber types contributing to dorsal root reflexes induced by joint inflammation in cats and monkeys. Journal of Neurophysiology. 1995, 74: 981-989.PubMed
42.
Lin Q, Zou X, Willis WD: Adelta and C Primary Afferents Convey Dorsal Root Reflexes After Intradermal Injection of Capsaicin in Rats. Journal of Neurophysiology. 2000, 84: 2695-2698.PubMed
43.
Peng YB, Wu J, Willis WD, Kenshalo DR: GABA(A) and 5-HT(3) receptors are involved in dorsal root reflexes: possible role in periaqueductal gray descending inhibition. Journal of Neurophysiology. 2001, 86: 49-58.PubMed
44.
Yaksh TL: Substance P release from knee joint afferent terminals: Modulation by opioids. Brain Research. 1988, 458: 319-324. 10.1016/0006-8993(88)90474-X.CrossRefPubMed
45.
Toennies JF: Reflex discharge from the spinal cord over the dorsal roots. Journal of Neurophysiology. 1938, 1: 378-390.
46.
Peng YB, Kenshalo DR, Gracely RH: Periaqueductal gray-evoked dorsal root reflex is frequency dependent. Brain Research. 2003, 976: 217-226. 10.1016/S0006-8993(03)02718-5.CrossRefPubMed
47.
Lobanov OV, Peng YB: Differential contribution of electrically-evoked dorsal root reflex to peripheral vasodilatation and plasma extravasation. Society for Neuroscience. 2006, 51: 11.
48.
Zimmermann M: Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983, 16: 109-110. 10.1016/0304-3959(83)90201-4.CrossRefPubMed
49.
Carmichael NM, Dostrovsky JO, Charlton MP: Enhanced vascular permeability in rat skin induced by sensory nerve stimulation: Evaluation of the time course and appropriate stimulation parameters. Neuroscience. 2008, 153: 832-841. 10.1016/j.neuroscience.2008.02.068.CrossRefPubMed
50.
Gonzalez HL, Carmichael N, Dostrovsky JO, Charlton MP: Evaluation of the time course of plasma extravasation in the skin by digital image analysis. Journal of Pain. 2005, 6: 681-688. 10.1016/j.jpain.2005.06.004.CrossRefPubMed
51.
Weng HR, Dougherty PM: Response properties of dorsal root reflexes in cutaneous C fibers before and after intradermal capsaicin injection in rats. Neuroscience. 2005, 132: 823-831. 10.1016/j.neuroscience.2005.01.039.CrossRefPubMed
52.
Bagust J, Kerkut GA, Rakkah NI: The dorsal root reflex in isolated mammalian spinal cord. Comp Biochem Physiol A. 1989, 93: 151-160. 10.1016/0300-9629(89)90202-8.CrossRefPubMed
53.
Bagust J, Chen Y, Kerkut GA: Spread of the dorsal root reflex in an isolated preparation of hamster spinal cord. Experimental Physiology. 1993, 78: 799-809.CrossRefPubMed
54.
Holzer P, Maggi CA: Dissociation of dorsal root ganglion neurons into afferent and efferent-like neurons. Neuroscience. 1998, 86: 389-398. 10.1016/S0306-4522(98)00047-5.CrossRefPubMed
55.
Hökfelt T, Kellerth JO, Nilsson G, Pernow B: Substance p: localization in the central nervous system and in some primary sensory neurons. Science. 1975, 190: 889-890.CrossRefPubMed
56.
Ishida-Yamamoto A, Senba E, Tohyama M: Distribution and fine structure of calcitonin gene-related peptide-like immunoreactive nerve fibers in the rat skin. Brain Research. 1989, 491: 93-101. 10.1016/0006-8993(89)90090-5.CrossRefPubMed
57.
Wu M, Komori N, Qin C, Farber JP, Linderoth B, Foreman RD: Roles of peripheral terminals of transient receptor potential vanilloid-1 containing sensory fibers in spinal cord stimulation-induced peripheral vasodilation. Brain Research. 2007, 1156: 80-92. 10.1016/j.brainres.2007.04.065.PubMedCentralCrossRefPubMed
58.
Fulop T, Radabaugh S, Smith C: Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. Journal of Neuroscience. 2005, 25: 7324-7332. 10.1523/JNEUROSCI.2042-05.2005.CrossRefPubMed
59.
Chan SA, Doreian B, Smith C: Dynamin and myosin regulate differential exocytosis from mouse adrenal chromaffin cells. Cell Mol Neurobiol. 2010, 30: 1351-1357. 10.1007/s10571-010-9591-z.PubMedCentralCrossRefPubMed
60.
Desarmenien M, Santangelo F, Loeffler JP, Feltz P: Comparative study of GABA-mediated depolarizations of lumbar A delta and C primary afferent neurones of the rat. Experimental Brain Research. 1984, 54: 521-528. 10.1007/BF00235477.CrossRefPubMed
61.
Gibbins IL, Wattchow D, Coventry B: Two immunohistochemically identified populations of calcitonin gene-related peptide (CGRP)-immunoreactive axons in human skin. Brain Research. 1987, 414: 143-148. 10.1016/0006-8993(87)91335-7.CrossRefPubMed
62.
Häbler HJ, Wasner G, Jänig W: Interaction of sympathetic vasoconstriction and antidromic vasodilatation in the control of skin blood flow. Experimental Brain Research. 1997, 113: 402-410.CrossRefPubMed
63.
Wang J, Ren Y, Zou X, Fang L, Willis WD, Lin Q: Sympathetic influence on capsaicin-evoked enhancement of dorsal root reflexes in rats. Journal of Neurophysiology. 2004, 92: 2017-2026. 10.1152/jn.00145.2004.CrossRefPubMed
64.
Lin Q, Zou X, Ren Y, Wang J, Fang L, Willis WD: Involvement of peripheral neuropeptide Y receptors in sympathetic modulation of acute cutaneous flare induced by intradermal capsaicin. Neuroscience. 2004, 123: 337-347. 10.1016/j.neuroscience.2003.09.017.CrossRefPubMed
Metadata
Title
Differential contribution of electrically evoked dorsal root reflexes to peripheral vasodilatation and plasma extravasation
Authors
Oleg V Lobanov
Yuan B Peng
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2011
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/1742-2094-8-20

Other articles of this Issue 1/2011

Journal of Neuroinflammation 1/2011 Go to the issue

Research

Fingolimod modulates microglial activation to augment markers of remyelination

Research

Reduced inflammation accompanies diminished myelin damage and repair in the NG2 null mouse spinal cord

Research

The effects of high dose interferon-β1a on plasma microparticles: Correlation with MRI parameters

Research

Insulin-like growth factor-I gene delivery to astrocytes reduces their inflammatory response to lipopolysaccharide

Research

Developmental regulation of the neuroinflammatory responses to LPS and/or hypoxia-ischemia between preterm and term neonates: An experimental study

Research

Gliovascular and cytokine interactions modulate brain endothelial barrier in vitro