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The Journal of Neurophysiology Vol. 84 No. 1 July 2000, pp. 205-215
Copyright ©2000 by the American Physiological Society
1Department of Cell and Animal Biology, Institute of Life Sciences, Hebrew University of Jerusalem, Jerusalem 91904, Israel; and 2Physiologisches Institut, Christian-Albrechts Universitat, 24098 Kiel, Germany
Liu, Chang-Ning,
Martin Michaelis,
Ron Amir, and
Marshall Devor.
Spinal Nerve Injury Enhances Subthreshold Membrane Potential
Oscillations in DRG Neurons: Relation to Neuropathic Pain. J. Neurophysiol. 84: 205-215, 2000. Primary sensory neurons with myelinated
axons were examined in vitro in excised whole lumbar dorsal root
ganglia (DRGs) taken from adult rats up to 9 days after tight ligation
and transection of the L5 spinal nerve (Chung
model of neuropathic pain). Properties of subthreshold membrane
potential oscillations, and of repetitive spike discharge, were
examined. About 5% of the DRG neurons sampled in control DRGs
exhibited high-frequency, subthreshold sinusoidal oscillations in their
membrane potential at rest (Vr), and
an additional 4.4% developed such oscillations on depolarization. Virtually all had noninflected action potentials
(A0 neurons). Amplitude and frequency of
subthreshold oscillations were voltage sensitive.
A0 neurons with oscillations at
Vr appear to constitute a population
distinct from A0 neurons that oscillate only on
depolarization. Axotomy triggered a significant increase in the
proportion of neurons exhibiting subthreshold oscillations both at
Vr and on depolarization. This change
occurred within a narrow time window 16-24 h postoperative. Axotomy
also shifted the membrane potential at which oscillation amplitude was
maximal to more negative (hyperpolarized) values, and lowered
oscillation frequency at any given membrane potential. Most neurons
that had oscillations at Vr, or that
developed them on depolarization, began to fire repetitively when
further depolarized. Spikes were triggered by the depolarizing phase of oscillatory sinusoids. Neurons that did not develop subthreshold oscillations never discharged repetitively and rarely fired more than a
single spike or a short burst, on step depolarization. The most
prominent spike waveform parameters distinguishing neurons capable of
generating subthreshold oscillations, and hence repetitive firing, was
their brief postspike afterhyperpolarization (AHP) and their low
single-spike threshold. Neurons that oscillated at
Vr tended to have a more prolonged
spike, with slower rise- and fall-time kinetics, and lower spike
threshold, than cells that oscillated only on depolarization. The main
effects of axotomy were to increase spike duration, slow rise- and
fall-time kinetics, and reduce single-spike threshold. Tactile
allodynia following spinal nerve injury is thought to result from
central amplification ("central sensitization") of afferent signals
entering the spinal cord from residual intact afferents. The central
sensitization, in turn, is thought to be triggered and maintained in
the Chung model by ectopic firing originating in the axotomized
afferent neurons. Axotomy by spinal nerve injury enhances subthreshold membrane potential oscillations in DRG neurons, augments ectopic discharge, and hence precipitates neuropathic pain.
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