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Journal of Neuroscience, Vol 15, 5943-5955, Copyright © 1995 by Society for Neuroscience
Retrograde synaptic communication via gap junctions coupling auditory afferents to the Mauthner cell
AE Pereda, TD Bell and DS Faber
Department of Anatomy and Neurobiology, Medical College of Pennsylvania, Philadelphia, USA.
Large myelinated club endings of the goldfish eighth nerve arise in the
sacculus and establish mixed electrotonic and chemical synapses with the
distal part of the Mauthner (M-) cell's lateral dendrite. We show here,
using paired pre- and postsynaptic recordings, that depolarizing currents
generated postsynaptically (specifically, the mixed synaptic potential
produced by activation of part of the afferent population) can in some
cases excite the presynaptic fibers and cause them to backfire. Strikingly,
while in some systems junctional properties prevent the antidromic spread
of depolarizing currents, physiological properties of these afferents and
the gap junctions promote backfiring: the amplitude of the coupling
potential recorded from an afferent fiber is voltage dependent, increasing
with depolarization and being reduced during hyperpolarization. Two
mechanisms, with different kinetics, underlie this voltage dependence. One,
a nonlinear membrane property of the afferent fiber itself, enhances the
coupling potential as the afferent membrane depolarizes. The second
mechanism, which is less sensitive to voltage and is symmetric about the
resting potential, most likely represents voltage dependence of the
junctional membrane. Additionally, we also show retrograde diffusion of low
molecular weight substances, as the fluorescent dye Lucifer yellow and the
tracer Neurobiotin were found in the terminals of afferent fibers after
being injected postsynaptically into the M-cell. These results suggest that
the gap junctions in these primary afferents are not only involved in fast
anterograde synaptic transmission but also provide the substrate for a
retrograde intercellular communication. The electrical coupling may modify
the input-output relation between eighth nerve afferents and the lateral
dendrite by synchronizing the population of already active fibers and by
promoting the recruitment of new fibers via backfiring, such that weaker
inputs produce relatively larger responses.
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