Phase Encoding in the Mauthner System: Implications in Left–Right Sound Source Discrimination

Abstract

The paired teleost Mauthner (M)-cells and their associated network serve as an excellent system to study the biophysical basis of decision making. In teleosts, an abrupt sound evokes an M-spike, triggering a C-start escape that is usually directed away from a sound source. The response latency is minimized by electrical synapses between auditory afferents and the M-cell lateral dendrite. Here, we demonstrate that the electrical synapses also mediate phase encoding. Ramped sound pressure waves (150-250 Hz) evoked electrotonic postsynaptic potentials in the M-cell locked to two diametrically opposed phase angles that were frequency dependent but intensity independent. Phase encoding was also evident at the behavioral level underwater, because the stimuli evoked directional C-starts with an onset that was phase locked to the sound wave. In interneurons inhibitory to the M-cell, these same stimuli also evoked phase-locked electrotonic postsynaptic potentials and action potentials. The resulting chemical and electrical (i.e., field effect) inhibitions functioned tonically and phasically, respectively. Phase encoding could be important in underwater sound source localization, which is thought to require a neural computation involving a phase comparison between the pressure and the directional particle motion components of sound. This computation may be implemented by an interplay between phase-dependent afferent excitation and feedforward inhibition that activates the appropriate M-cell and directs the C-start away from the sound source.