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Volume 16, Number 15,
Issue of August 1, 1996
pp. 4733-4741
Copyright ©1996 Society for Neuroscience
Chemically Mediated Cross-Excitation in Rat Dorsal Root
Ganglia
Received Jan. 23, 1996; revised May 3, 1996; accepted May 13, 1996.
Ron Amir and
Marshall Devor
Department of Cell and Animal Biology, Life Sciences Institute,
Hebrew University of Jerusalem, Jerusalem 91904, Israel
Primary afferent neurons in mammalian dorsal root ganglia (DRGs)
are anatomically isolated from one another and are not synaptically
interconnected. As such, they are classically thought to function as
independent sensory communication elements. However, it has recently
been shown that most DRG neurons are transiently depolarized when axons
of neighboring neurons of the same ganglion are stimulated
repetitively. Here we further characterize this functional coupling. In
electrophysiological recordings made from excised rat DRGs, we found
that DRG ``cross-depolarization'' is excitatory in that it is
accompanied by an increase in the probability of spiking in response to
otherwise subthreshold test pulses delivered intracellularly.
Cross-depolarization contributes to this mutual cross-excitation.
However, at least as important a contribution comes from a net increase
in the neurons' input resistance (Rin)
triggered by the stimulation of neighboring neurons. This change in
Rin occurs even when cross-depolarization
is absent or is balanced out. The amplitude of cross-depolarization was
found to be voltage-dependent, with a reversal potential at
approximately 23 mV. Reversibility and the change in
Rin both indicate that activity of
neighboring neurons causes a membrane conductance change that is
chemically mediated. Thus, far from being isolated, most DRG neurons
participate in ongoing mutual interactions in which neuronal
excitability is continuously modulated by afferent spike activity. This
intraganglionic dialog appears to be mediated, at least in part, by an
activity-dependent diffusable substance(s) released from neuronal
somata and/or adjacent axons, and detected by neighboring cell somata
and/or axons.
Key words:
cross-excitation;
cross talk;
dorsal root
ganglion;
neuropathy;
nonsynaptic neurotransmission;
pain
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