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The Journal of Neurophysiology Vol. 85 No. 2 February 2001, pp. 630-643
Copyright ©2001 by the American Physiological Society
1Department of Pharmacology and Division of Neuroscience, University of Alberta, Edmonton, Alberta T6G 2H7, Canada; and 2Department of Physical Therapy, Tennessee State University, Nashville, Tennessee 37209
Abdulla, Fuad A. and
Peter A. Smith.
Axotomy- and Autotomy-Induced Changes in the Excitability of Rat
Dorsal Root Ganglion Neurons. J. Neurophysiol. 85: 630-643, 2001. The spontaneous, ectopic activity in
sensory nerves that is induced by peripheral nerve injury is thought to
contribute to the generation of "neuropathic" pain in humans. To
examine the cellular mechanisms that underlie this activity, neurons in
rat L4-L5 dorsal root
ganglion (DRG) were first grouped as "large," "medium," or
"small" on the basis of their size (input capacitance) and action
potential (AP) shape. A fourth group of cells that exhibited a
pronounced afterdepolarization (ADP) were defined as AD-cells. Whole
cell recording was used to compare the properties of control neurons
with those dissociated from rats in which the sciatic nerve had been
sectioned ("axotomy" group) and with neurons from rats that
exhibited self-mutilatory behavior in response to sciatic nerve section
("autotomy" group). Increases in excitability in all types of DRG
neuron were seen within 2-7 wk of axotomy. Resting membrane potential
(RMP) and the amplitude and duration of the afterhyperpolarization
(AHP) that followed the AP were unaffected. Effects of axotomy were
greatest in the small, putative nociceptive cells and least in the
large cells. Moderate changes were seen in the medium and AD-cells.
Compared to control neurons, axotomized neurons exhibited a higher
frequency of evoked AP discharge in response to 500-ms depolarizing
current injections; i.e., "gain" was increased and accommodation
was decreased. The minimum current required to discharge an AP
(rheobase) was reduced. There were significant increases in spike width
in small cells and significant increases in spike height in small,
medium, and AD-cells. The electrophysiological changes promoted by
axotomy were intensified in animals that exhibited autotomy; spike
height, and spike width were significantly greater than control for all
cell types. Under our experimental conditions, spontaneous activity was
never encountered in neurons dissociated from animals that exhibited
autotomy. Thus changes in the electrical properties of cell bodies
alone may not entirely account for injury-induced
spontaneous activity in sensory nerves. The onset of autotomy coincided
with alterations in the excitability of large, putative nonnociceptive,
neurons. Thus large cells from the autotomy group were much
more excitable than those from the axotomy group, whereas small cells
from the autotomy group were only slightly more excitable.
This is consistent with the hypothesis that the onset of autotomy is
associated with changes in the properties of myelinated fibers. Changes
in Ca2+ and K+ channel
conductances that contribute to axotomy- and autotomy-induced changes
in excitability are addressed in the accompanying paper.
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