Peripheral Nerve Injury Alters Excitatory Synaptic Transmission in Lamina II of the Rat Dorsal Horn

Overview

Journal J Physiol

Specialty Physiology

Date 2003 Feb 11

PMID 12576493

Citations 59

Authors

Tatsuro Kohno

Kimberly A Moore

Hiroshi Baba

Clifford J Woolf

Affiliations

Soon will be listed here.

Abstract

Using the blind whole cell patch-clamp recording technique, we investigated peripheral nerve injury-induced changes in excitatory synaptic transmission to neurones in lamina II of the dorsal horn. Partial (i.e. chronic constriction injury (CCI) and spared nerve injury (SNI)) and complete (i.e. sciatic nerve transection (SNT)) peripheral nerve injury altered the mean threshold intensity for eliciting A fibre-mediated EPSCs in lamina II neurones. Following SNT and CCI, EPSC threshold was significantly decreased, but following SNI, EPSC threshold was increased (naive: 32 +/- 2 mu A, SNT: 22 +/- 2 mu A, CCI: 23 +/- 2 mu A, SNI: 49 +/- 4 mu A; P < 0.01, Student's unpaired t test). Despite this disparity between models, dorsal root compound action potential recordings revealed no significant difference in the conduction velocity or activation threshold of A beta and A delta fibres in naive, SNT, CCI and SNI rats. In addition to the changes in EPSC threshold, we also observed a shift in the distribution of EPSCs. In spinal cord slices from naive rats, polysynaptic A beta fibre-evoked EPSCs were observed in 24 % of lamina II neurones, monosynaptic A delta fibre EPSCs were observed in 34 % and polysynaptic A delta fibre EPSCs were observed in 7 %. Following SNT and CCI, the percentage of neurones with polysynaptic A beta fibre EPSCs increased to > or = 65 % of the sampled population, while the percentage of neurones with monosynaptic A delta fibre EPSCs decreased to < 10 %. The percentage of neurones with polysynaptic A delta fibre EPSCs was unchanged. In contrast, following SNI, A beta fibre EPSCs decreased in incidence while the percentage of neurones with polysynaptic A delta fibre EPSCs increased to 44 %. Similar to the other injury models, however, monosynaptic A delta fibre EPSCs decreased in frequency following SNI. Thus, excitatory synaptic transmission is subject to divergent plasticity in different peripheral nerve injury models, reflecting the complexity of responses to different forms of deafferentation.

Citing Articles

Visualizing the modulation of neurokinin 1 receptor-positive neurons in the superficial dorsal horn by spinal cord stimulation in vivo.

Xu Q, Zheng Q, Cui X, Cleland A, Hincapie J, Raja S Pain. 2024; 166(2):428-437.

PMID: 39140483 PMC: 11723817. DOI: 10.1097/j.pain.0000000000003361.

Structural and functional properties of spinal dorsal horn neurons after peripheral nerve injury change overtime via astrocyte activation.

Kurabe M, Sasaki M, Furutani K, Furue H, Kamiya Y, Baba H iScience. 2022; 25(12):105555.

PMID: 36444301 PMC: 9700017. DOI: 10.1016/j.isci.2022.105555.

Kappa opioids inhibit the GABA/glycine terminals of rostral ventromedial medulla projections in the superficial dorsal horn of the spinal cord.

Otsu Y, Aubrey K J Physiol. 2022; 600(18):4187-4205.

PMID: 35979937 PMC: 9540474. DOI: 10.1113/JP283021.

Altered synaptic connections and inhibitory network of the primary somatosensory cortex in chronic pain.

Kim Y, Kim S Korean J Physiol Pharmacol. 2022; 26(2):69-75.

PMID: 35203057 PMC: 8890942. DOI: 10.4196/kjpp.2022.26.2.69.

Needling Interventions for Sciatica: Choosing Methods Based on Neuropathic Pain Mechanisms-A Scoping Review.

Perreault T, Fernandez-de-Las-Penas C, Cummings M, Gendron B J Clin Med. 2021; 10(10).

PMID: 34069357 PMC: 8158699. DOI: 10.3390/jcm10102189.

References

Ataka T, Kumamoto E, Shimoji K, Yoshimura M . Baclofen inhibits more effectively C-afferent than Adelta-afferent glutamatergic transmission in substantia gelatinosa neurons of adult rat spinal cord slices. Pain. 2000; 86(3):273-282. DOI: 10.1016/S0304-3959(00)00255-4. View

Kapadia S, LaMotte C . Deafferentation-induced alterations in the rat dorsal horn: I. Comparison of peripheral nerve injury vs. rhizotomy effects on presynaptic, postsynaptic, and glial processes. J Comp Neurol. 1987; 266(2):183-97. DOI: 10.1002/cne.902660205. View

Nakamura S, Myers R . Myelinated afferents sprout into lamina II of L3-5 dorsal horn following chronic constriction nerve injury in rats. Brain Res. 1999; 818(2):285-90. DOI: 10.1016/s0006-8993(98)01291-8. View

Decosterd I, Woolf C . Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain. 2000; 87(2):149-158. DOI: 10.1016/S0304-3959(00)00276-1. View

Koerber H, Mirnics K, Kavookjian A, Light A . Ultrastructural analysis of ectopic synaptic boutons arising from peripherally regenerated primary afferent fibers. J Neurophysiol. 1999; 81(4):1636-44. DOI: 10.1152/jn.1999.81.4.1636. View

Kohama I, Ishikawa K, Kocsis J . Synaptic reorganization in the substantia gelatinosa after peripheral nerve neuroma formation: aberrant innervation of lamina II neurons by Abeta afferents. J Neurosci. 2000; 20(4):1538-49. PMC: 2605372. View

Shortland P, Woolf C, Fitzgerald M . Morphology and somatotopic organization of the central terminals of hindlimb hair follicle afferents in the rat lumbar spinal cord. J Comp Neurol. 1989; 289(3):416-33. DOI: 10.1002/cne.902890307. View

Nakatsuka T, Ataka T, Kumamoto E, Tamaki T, Yoshimura M . Alteration in synaptic inputs through C-afferent fibers to substantia gelatinosa neurons of the rat spinal dorsal horn during postnatal development. Neuroscience. 2000; 99(3):549-56. DOI: 10.1016/s0306-4522(00)00224-4. View

Basbaum A, Gautron M, Jazat F, Mayes M, Guilbaud G . The spectrum of fiber loss in a model of neuropathic pain in the rat: an electron microscopic study. Pain. 1991; 47(3):359-367. DOI: 10.1016/0304-3959(91)90229-Q. View

10.

Ma Q, Tian L . A-fibres sprouting from lamina I into lamina II of spinal dorsal horn after peripheral nerve injury in rats. Brain Res. 2001; 904(1):137-40. DOI: 10.1016/s0006-8993(01)02420-9. View

11.

Moore K, Kohno T, Karchewski L, Scholz J, Baba H, Woolf C . Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J Neurosci. 2002; 22(15):6724-31. PMC: 6758148. DOI: 20026611. View

12.

Koerber H, Mirnics K, Brown P, Mendell L . Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci. 1994; 14(6):3655-71. PMC: 6576924. View

13.

Woolf C, Shortland P, Reynolds M, Ridings J, Doubell T, Coggeshall R . Reorganization of central terminals of myelinated primary afferents in the rat dorsal horn following peripheral axotomy. J Comp Neurol. 1995; 360(1):121-34. DOI: 10.1002/cne.903600109. View

14.

Yoshimura M, Nishi S . Blind patch-clamp recordings from substantia gelatinosa neurons in adult rat spinal cord slices: pharmacological properties of synaptic currents. Neuroscience. 1993; 53(2):519-26. DOI: 10.1016/0306-4522(93)90216-3. View

15.

Villiere V, McLachlan E . Electrophysiological properties of neurons in intact rat dorsal root ganglia classified by conduction velocity and action potential duration. J Neurophysiol. 1996; 76(3):1924-41. DOI: 10.1152/jn.1996.76.3.1924. View

16.

Baba H, Doubell T, Moore K, Woolf C . Silent NMDA receptor-mediated synapses are developmentally regulated in the dorsal horn of the rat spinal cord. J Neurophysiol. 2000; 83(2):955-62. DOI: 10.1152/jn.2000.83.2.955. View

17.

Baba H, Doubell T, Woolf C . Peripheral inflammation facilitates Abeta fiber-mediated synaptic input to the substantia gelatinosa of the adult rat spinal cord. J Neurosci. 1999; 19(2):859-67. PMC: 6782212. View

18.

Okamoto M, Baba H, Goldstein P, Higashi H, Shimoji K, Yoshimura M . Functional reorganization of sensory pathways in the rat spinal dorsal horn following peripheral nerve injury. J Physiol. 2001; 532(Pt 1):241-50. PMC: 2278535. DOI: 10.1111/j.1469-7793.2001.0241g.x. View

19.

Kohno T, Kumamoto E, Higashi H, Shimoji K, Yoshimura M . Actions of opioids on excitatory and inhibitory transmission in substantia gelatinosa of adult rat spinal cord. J Physiol. 1999; 518 ( Pt 3):803-13. PMC: 2269468. DOI: 10.1111/j.1469-7793.1999.0803p.x. View

20.

Bennett G, Xie Y . A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain. 1988; 33(1):87-107. DOI: 10.1016/0304-3959(88)90209-6. View