Representation of auditory signals in the M-cell: role of electrical synapses

The teleost Mauthner (M-) cell mediates a sound-evoked escape behavior. A major component of the auditory input is transmitted by large myelinated club endings of the posterior VIIIth nerve. Paradoxically, although nerve stimulations revealed these afferents have mixed electrical and glutamatergic synapses on the M-cell's distal lateral dendrite, paired pre- and postsynaptic recordings indicated most individual connections are chemically silent. To determine the sensory information encoded and the relative contributions of these two transmission modes, M-cell responses to acoustic stimuli in air were recorded intracellularly. Excitatory postsynaptic potentials (EPSPs) evoked by both short 100- to 900-Hz "pips" and longer-lasting amplitude- and frequency-modulated sounds were dominated by fast, repetitive EPSPs superimposed on an underlying slow depolarization. Fast EPSPs 1) have kinetics comparable to presynaptic action potentials, 2) are maximal on the distal lateral dendrite, and 3) are insensitive to GluR antagonists. They presumably are coupling potentials, and power spectral analysis indicated they constitute a high-pass signal that accurately tracks sound frequency and amplitude. The spatial profile of the slow EPSP suggests both proximal and distal dendritic sources, a result supported by predictions of a multicompartmental model and the effects of AMPAR antagonists, which preferentially reduced the proximal component. Thus a second class of afferents generates a portion of the slow EPSP that, with sound stimuli, demonstrate that the dominant mode of transmission at LMCE synapses is electrical. The slow EPSP is a dynamic, low-pass representation of stimulus strength. Accordingly, amplitude and phase information, which are segregated in other systems, are faithfully represented in the M-cell.