RETROGRADE SYNAPTIC COMMUNICATION VIA GAP JUNCTION COUPLING AUDITORY AFFERENTS TO THE MAUTHNER CELL

Large myelinated club endings of the goldfish eighth nerve arise in th e 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 depolarizin g currents generated postsynaptically (specifically, the mixed synapti c potential produced by activation of part of the afferent population) can in some cases excite the presynaptic fibers and cause them to bac kfire, Strikingly, while in some systems junctional properties prevent the antidromic spread of depolarizing currents, physiological propert ies of these afferents and the gap junctions promote backfiring: the a mplitude of the coupling potential recorded from an afferent fiber is voltage dependent, increasing with depolarization and being reduced du ring hyperpolarization, Two mechanisms, with different kinetics, under lie this voltage dependence, One, a nonlinear membrane property of the afferent fiber itself, enhances the coupling potential as the afferen t membrane depolarizes, The second mechanism, which is less sensitive to voltage and is symmetric about the resting potential, most likely r epresents 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 postsy naptically into the M-cell. These results suggest that the gap junctio ns in these primary afferents are not only involved in fast anterograd e synaptic transmission but also provide the substrate for a retrograd e intercellular communication, The electrical coupling may modify the input-output relation between eighth nerve afferents and the lateral d endrite by synchronizing the population of already active; fibers and by promoting the recruitment of new fibers via backfiring, such that w eaker inputs produce relatively larger responses.