Ectopic excitability of injured nerves in monkey: Entrained responses to vibratory stimuli

G. M. Koschorke, Richard Meyer, D. B. Tillman, James N Campbell

Research output: Contribution to journalArticle

Abstract

The responses to mechanical stimulation of myelinated fibers that originate from an acutely cut nerve or a neuroma were studied in the anesthetized monkey. The superficial radial or sural nerve was tightly ligated and cut. Either immediately (acute experiment) or 2-6 wk later (chronic experiment), single-unit recording techniques were used to record the evoked neural activity after vibratory mechanical stimulation (5-100 Hz; 50-800 μm) near the injury site. The 30 myelinated afferents studied in the chronic experiments displayed an entrained response (1 action potential for each stimulus cycle) to vibratory stimuli applied at or near the nerve injury site. For 19 fibers, the minimum amplitude for entrainment was determined as a function of frequency (tuning curve). For 11 others, complete tuning curves were not obtained, although the frequency range over which they were most sensitive could be estimated. The afferents could be classified into three groups on the basis of the frequency range over which they were most sensitive: 1) a low-frequency group that was most sensitive to frequencies ≤5 Hz (n = 7), 2) a mid-frequency group that was most sensitive to a broad range of frequencies (i.e., 20-75 Hz, n = 13), and 3) a high-frequency group that was most sensitive to frequencies ≥100 Hz (n = 10). These three response classes are similar to the three classes of response associated with the different low-threshold mechanoreceptors (i.e., slowly and rapidly adapting and Pacinian-like mechanoreceptors. In the acute experiments, the nerve was either kept warm (38°C, n = 6) or cold (28°C, n = 4) after the nerve ligation. In the warm experiments, mechanical sensitivity first developed within 4 h of the injury, and 23% of the myelinated fibers were mechanically sensitive 10 h after the ligation. In contrast, mechanical sensitivity was not apparent until 6 h after the injury in the cold experiments, and only 7% of the myelinated fibers were mechanically sensitive after 10 h. Seven days after an injury to the common peroneal nerve, none of the 63 A-fibers from the ventral root that could be activated electrically at the nerve injury site were mechanically sensitive. In contrast, 47% of the A-fibers from the dorsal root were mechanically sensitive. This suggests that mechanosensitivity is a specific property of sensory fibers. Intact nerves did not demonstrate sensitivity to vibratory stimuli. In addition, when centrifugally conducted action potentials were recorded 12 h after a proximal nerve injury, only 1% of the A-fibers were mechanically sensitive. We postulate that the cellular components necessary for mechanical-to-electrical transduction are conveyed to the low-threshold mechanoreceptors via axonal transport. These components accumulate at a nerve injury site and are incorporated into the membrane to impart ectopic sensitivity.

Original languageEnglish (US)
Pages (from-to)693-701
Number of pages9
JournalJournal of Neurophysiology
Volume65
Issue number3
StatePublished - 1991

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Haplorhini
Myelinated Nerve Fibers
Wounds and Injuries
Mechanoreceptors
Spinal Nerve Roots
Action Potentials
Ligation
Neuroma
Radial Nerve
Sural Nerve
Peroneal Nerve
Axonal Transport
Membranes

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Ectopic excitability of injured nerves in monkey : Entrained responses to vibratory stimuli. / Koschorke, G. M.; Meyer, Richard; Tillman, D. B.; Campbell, James N.

In: Journal of Neurophysiology, Vol. 65, No. 3, 1991, p. 693-701.

Research output: Contribution to journalArticle

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abstract = "The responses to mechanical stimulation of myelinated fibers that originate from an acutely cut nerve or a neuroma were studied in the anesthetized monkey. The superficial radial or sural nerve was tightly ligated and cut. Either immediately (acute experiment) or 2-6 wk later (chronic experiment), single-unit recording techniques were used to record the evoked neural activity after vibratory mechanical stimulation (5-100 Hz; 50-800 μm) near the injury site. The 30 myelinated afferents studied in the chronic experiments displayed an entrained response (1 action potential for each stimulus cycle) to vibratory stimuli applied at or near the nerve injury site. For 19 fibers, the minimum amplitude for entrainment was determined as a function of frequency (tuning curve). For 11 others, complete tuning curves were not obtained, although the frequency range over which they were most sensitive could be estimated. The afferents could be classified into three groups on the basis of the frequency range over which they were most sensitive: 1) a low-frequency group that was most sensitive to frequencies ≤5 Hz (n = 7), 2) a mid-frequency group that was most sensitive to a broad range of frequencies (i.e., 20-75 Hz, n = 13), and 3) a high-frequency group that was most sensitive to frequencies ≥100 Hz (n = 10). These three response classes are similar to the three classes of response associated with the different low-threshold mechanoreceptors (i.e., slowly and rapidly adapting and Pacinian-like mechanoreceptors. In the acute experiments, the nerve was either kept warm (38°C, n = 6) or cold (28°C, n = 4) after the nerve ligation. In the warm experiments, mechanical sensitivity first developed within 4 h of the injury, and 23{\%} of the myelinated fibers were mechanically sensitive 10 h after the ligation. In contrast, mechanical sensitivity was not apparent until 6 h after the injury in the cold experiments, and only 7{\%} of the myelinated fibers were mechanically sensitive after 10 h. Seven days after an injury to the common peroneal nerve, none of the 63 A-fibers from the ventral root that could be activated electrically at the nerve injury site were mechanically sensitive. In contrast, 47{\%} of the A-fibers from the dorsal root were mechanically sensitive. This suggests that mechanosensitivity is a specific property of sensory fibers. Intact nerves did not demonstrate sensitivity to vibratory stimuli. In addition, when centrifugally conducted action potentials were recorded 12 h after a proximal nerve injury, only 1{\%} of the A-fibers were mechanically sensitive. We postulate that the cellular components necessary for mechanical-to-electrical transduction are conveyed to the low-threshold mechanoreceptors via axonal transport. These components accumulate at a nerve injury site and are incorporated into the membrane to impart ectopic sensitivity.",
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