Effects of electrical and mechanical stimulation on two foci of spontaneous activity which develop in primary afferent neurons after peripheral axotomy

Research output: Contribution to journalArticle

96 Citations (Scopus)

Abstract

In 28 Sprague-Dawley rats, unilateral division of the sciatic nerve at the level of the midfemur was performed. Animals were observed for behavioral changes for 1-21 days, and electrophysiological recordings were made from microfilaments dissected from the ipsilateral L5 dorsal rootlets and sciatic nerve from 1 to 14 days postoperatively. Spontaneous discharges of two types were recorded: (1) variable frequency (0-100 Hz) discharges which typically occurred in rhythmic bursts and could be driven by mechanical stimulation of the neuroma; and (2) lower frequency (0.25-14 Hz) irregular activity which persisted after either excision or local anesthesia of the neuroma. The latter activity could also be recorded from the proximal cut end of the sciatic nerve following removal of the neuroma. The first type of activity was felt to be produced from the neuroma while the second originated in the region of the dorsal root ganglion (DRG). Analysis of the conduction velocities of fibers involved in each type of discharge indicated that both involved smaller myelinated filaments. However, the DRG activity involved significantly smaller fibers with conduction velocities in the Aδ range. Spontaneous activity was recorded at 3 and 4 days for the neuroma and DRG activity, respectively. Ongoing discharges maximized at 7-10 days and were rare by 14 days. Autotomy of the ipsilateral foot was found to occur over a similar time course. Tetanic electrical stimulation (100 Hz) produced either little change in the baseline firing rate or prolonged afterdischarges in fibers manifesting neuroma activity. In fibers with ongoing activity of DRG origin, stimulation produced a stereotyped, brief low-frequency afterburst and then prolonged inhibition of firing. Mechanical stimulation of the neuroma produced both brief increases in spontaneous discharges and prolonged afterdischarges. In fibers with spontaneous DRG activity, minimal mechanical stimulation of their ganglion of origin produced prolonged high-frequency firing. This study demonstrates that peripheral axotomy of DRG neurons produces spontaneous activity distinct from ongoing neuroma activity in a proportion of fibers which are potentially nociceptive (Aδ) as well as abnormal mechanosensitivity of the DRG. Furthermore, electrical stimulation of these fibers produces prolonged inhibition of the discharge. This finding may partially explain the prolonged relief of symptoms patients with chronic pain of peripheral origin may experience following peripheral tetanic electrical stimulation.

Original languageEnglish (US)
Pages (from-to)249-265
Number of pages17
JournalPain
Volume18
Issue number3
DOIs
StatePublished - 1984
Externally publishedYes

Fingerprint

Neuroma
Axotomy
Afferent Neurons
Spinal Ganglia
Electric Stimulation
Sciatic Nerve
Local Anesthesia
Actin Cytoskeleton
Ganglia
Chronic Pain
Sprague Dawley Rats
Foot
Neurons

ASJC Scopus subject areas

  • Clinical Neurology
  • Psychiatry and Mental health
  • Neuroscience(all)
  • Neurology
  • Pharmacology
  • Clinical Psychology

Cite this

@article{9ddad86a8b824b9f93095827751eaa6d,
title = "Effects of electrical and mechanical stimulation on two foci of spontaneous activity which develop in primary afferent neurons after peripheral axotomy",
abstract = "In 28 Sprague-Dawley rats, unilateral division of the sciatic nerve at the level of the midfemur was performed. Animals were observed for behavioral changes for 1-21 days, and electrophysiological recordings were made from microfilaments dissected from the ipsilateral L5 dorsal rootlets and sciatic nerve from 1 to 14 days postoperatively. Spontaneous discharges of two types were recorded: (1) variable frequency (0-100 Hz) discharges which typically occurred in rhythmic bursts and could be driven by mechanical stimulation of the neuroma; and (2) lower frequency (0.25-14 Hz) irregular activity which persisted after either excision or local anesthesia of the neuroma. The latter activity could also be recorded from the proximal cut end of the sciatic nerve following removal of the neuroma. The first type of activity was felt to be produced from the neuroma while the second originated in the region of the dorsal root ganglion (DRG). Analysis of the conduction velocities of fibers involved in each type of discharge indicated that both involved smaller myelinated filaments. However, the DRG activity involved significantly smaller fibers with conduction velocities in the Aδ range. Spontaneous activity was recorded at 3 and 4 days for the neuroma and DRG activity, respectively. Ongoing discharges maximized at 7-10 days and were rare by 14 days. Autotomy of the ipsilateral foot was found to occur over a similar time course. Tetanic electrical stimulation (100 Hz) produced either little change in the baseline firing rate or prolonged afterdischarges in fibers manifesting neuroma activity. In fibers with ongoing activity of DRG origin, stimulation produced a stereotyped, brief low-frequency afterburst and then prolonged inhibition of firing. Mechanical stimulation of the neuroma produced both brief increases in spontaneous discharges and prolonged afterdischarges. In fibers with spontaneous DRG activity, minimal mechanical stimulation of their ganglion of origin produced prolonged high-frequency firing. This study demonstrates that peripheral axotomy of DRG neurons produces spontaneous activity distinct from ongoing neuroma activity in a proportion of fibers which are potentially nociceptive (Aδ) as well as abnormal mechanosensitivity of the DRG. Furthermore, electrical stimulation of these fibers produces prolonged inhibition of the discharge. This finding may partially explain the prolonged relief of symptoms patients with chronic pain of peripheral origin may experience following peripheral tetanic electrical stimulation.",
author = "Kim Burchiel",
year = "1984",
doi = "10.1016/0304-3959(84)90820-0",
language = "English (US)",
volume = "18",
pages = "249--265",
journal = "Pain",
issn = "0304-3959",
publisher = "Elsevier",
number = "3",

}

TY - JOUR

T1 - Effects of electrical and mechanical stimulation on two foci of spontaneous activity which develop in primary afferent neurons after peripheral axotomy

AU - Burchiel, Kim

PY - 1984

Y1 - 1984

N2 - In 28 Sprague-Dawley rats, unilateral division of the sciatic nerve at the level of the midfemur was performed. Animals were observed for behavioral changes for 1-21 days, and electrophysiological recordings were made from microfilaments dissected from the ipsilateral L5 dorsal rootlets and sciatic nerve from 1 to 14 days postoperatively. Spontaneous discharges of two types were recorded: (1) variable frequency (0-100 Hz) discharges which typically occurred in rhythmic bursts and could be driven by mechanical stimulation of the neuroma; and (2) lower frequency (0.25-14 Hz) irregular activity which persisted after either excision or local anesthesia of the neuroma. The latter activity could also be recorded from the proximal cut end of the sciatic nerve following removal of the neuroma. The first type of activity was felt to be produced from the neuroma while the second originated in the region of the dorsal root ganglion (DRG). Analysis of the conduction velocities of fibers involved in each type of discharge indicated that both involved smaller myelinated filaments. However, the DRG activity involved significantly smaller fibers with conduction velocities in the Aδ range. Spontaneous activity was recorded at 3 and 4 days for the neuroma and DRG activity, respectively. Ongoing discharges maximized at 7-10 days and were rare by 14 days. Autotomy of the ipsilateral foot was found to occur over a similar time course. Tetanic electrical stimulation (100 Hz) produced either little change in the baseline firing rate or prolonged afterdischarges in fibers manifesting neuroma activity. In fibers with ongoing activity of DRG origin, stimulation produced a stereotyped, brief low-frequency afterburst and then prolonged inhibition of firing. Mechanical stimulation of the neuroma produced both brief increases in spontaneous discharges and prolonged afterdischarges. In fibers with spontaneous DRG activity, minimal mechanical stimulation of their ganglion of origin produced prolonged high-frequency firing. This study demonstrates that peripheral axotomy of DRG neurons produces spontaneous activity distinct from ongoing neuroma activity in a proportion of fibers which are potentially nociceptive (Aδ) as well as abnormal mechanosensitivity of the DRG. Furthermore, electrical stimulation of these fibers produces prolonged inhibition of the discharge. This finding may partially explain the prolonged relief of symptoms patients with chronic pain of peripheral origin may experience following peripheral tetanic electrical stimulation.

AB - In 28 Sprague-Dawley rats, unilateral division of the sciatic nerve at the level of the midfemur was performed. Animals were observed for behavioral changes for 1-21 days, and electrophysiological recordings were made from microfilaments dissected from the ipsilateral L5 dorsal rootlets and sciatic nerve from 1 to 14 days postoperatively. Spontaneous discharges of two types were recorded: (1) variable frequency (0-100 Hz) discharges which typically occurred in rhythmic bursts and could be driven by mechanical stimulation of the neuroma; and (2) lower frequency (0.25-14 Hz) irregular activity which persisted after either excision or local anesthesia of the neuroma. The latter activity could also be recorded from the proximal cut end of the sciatic nerve following removal of the neuroma. The first type of activity was felt to be produced from the neuroma while the second originated in the region of the dorsal root ganglion (DRG). Analysis of the conduction velocities of fibers involved in each type of discharge indicated that both involved smaller myelinated filaments. However, the DRG activity involved significantly smaller fibers with conduction velocities in the Aδ range. Spontaneous activity was recorded at 3 and 4 days for the neuroma and DRG activity, respectively. Ongoing discharges maximized at 7-10 days and were rare by 14 days. Autotomy of the ipsilateral foot was found to occur over a similar time course. Tetanic electrical stimulation (100 Hz) produced either little change in the baseline firing rate or prolonged afterdischarges in fibers manifesting neuroma activity. In fibers with ongoing activity of DRG origin, stimulation produced a stereotyped, brief low-frequency afterburst and then prolonged inhibition of firing. Mechanical stimulation of the neuroma produced both brief increases in spontaneous discharges and prolonged afterdischarges. In fibers with spontaneous DRG activity, minimal mechanical stimulation of their ganglion of origin produced prolonged high-frequency firing. This study demonstrates that peripheral axotomy of DRG neurons produces spontaneous activity distinct from ongoing neuroma activity in a proportion of fibers which are potentially nociceptive (Aδ) as well as abnormal mechanosensitivity of the DRG. Furthermore, electrical stimulation of these fibers produces prolonged inhibition of the discharge. This finding may partially explain the prolonged relief of symptoms patients with chronic pain of peripheral origin may experience following peripheral tetanic electrical stimulation.

UR - http://www.scopus.com/inward/record.url?scp=0021347435&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0021347435&partnerID=8YFLogxK

U2 - 10.1016/0304-3959(84)90820-0

DO - 10.1016/0304-3959(84)90820-0

M3 - Article

VL - 18

SP - 249

EP - 265

JO - Pain

JF - Pain

SN - 0304-3959

IS - 3

ER -