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The Journal of Neuroscience, February 1, 2002, 22(3):1187-1198
Burst Discharge in Primary Sensory Neurons: Triggered by
Subthreshold Oscillations, Maintained by Depolarizing
Afterpotentials
Ron
Amir1,
Martin
Michaelis2, and
Marshall
Devor1
1 Department of Cell and Animal Biology, Institute of
Life Sciences, Hebrew University of Jerusalem, Jerusalem 91904, Israel,
and 2 Physiologisches Institut, Christian-Albrechts
Universitat, 24098 Kiel, Germany
Afferent discharge generated ectopically in the cell soma of dorsal
root ganglion (DRG) neurons may play a role in normal sensation, and it
contributes to paraesthesias and pain after nerve trauma. This activity
is critically dependent on subthreshold membrane potential
oscillations; oscillatory sinusoids that reach threshold trigger
low-frequency trains of intermittent spikes. Ectopic firing may also
enter a high-frequency bursting mode, however, particularly in the
event of neuropathy. Bursting greatly amplifies the overall ectopic
barrage. In the present report we show that subthreshold oscillations
and burst discharge occur in vivo, as they do in
vitro. We then show that although the first spike in each burst
is triggered by an oscillatory sinusoid, firing within bursts is
maintained by brief regenerative post-spike depolarizing afterpotentials (DAPs). Numerical simulations were used to identify the
cellular process underlying rebound DAPs, and hence the mechanism of
the spike bursts. Finally, we show that slow ramp and hold (tonic)
depolarizations of the sort that occur in DRG neurons during
physiologically relevant events are capable of triggering sustained
ectopic bursting, but only in cells with subthreshold oscillatory
behavior. Oscillations and DAPs are an essential substrate of ectopic
burst discharge. Therefore, any consideration of the ways in which
cellular regulation of ion channel synthesis and trafficking implement
normal sensation and, when disrupted, bring about neuropathic pain must
take into account the effects of this regulation on oscillations and bursting.
Key words:
depolarizing afterpotential; dorsal root ganglion; ectopic firing; neuropathic pain; pain; paresthesia; subthreshold
oscillations
Copyright © 2002 Society for Neuroscience 0270-6474/02/2231187-12$05.00/0
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