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 [lumbar] L5 dorsal rootlets and sciatic nerve from 1-14 days postoperatively. Spontaneous discharges of 2 types were recorded: variable frequency (0-100 Hz) discharges which typically occurred in rhythmic bursts and could be driven by mechanical stimulation of the neuroma and lower frequency (0.25-14 Hz) irregular activity which persisted after either excision or local anesthesia of the neuroma. Th latter activity could also be recorded from the proximal cut end of the sciatic nerve following removal of the neuroma. The 1st type of activity was produced from the neuroma while the 2nd 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. The DRG activity involved significantly smaller fibers with conduction velocities in the A.delta. 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. Peripheral axotomy of DRG neurons produces spontaneous activity distinct from ongoing neuroma activity in a proportion of fibers which are potentially nociceptive (A.delta.) as well as abnormal mechanosensitivity of the DRG. 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.