Interplay between subthreshold potentials and γ oscillations in Mauthner cells’ presynaptic inhibitory interneurons

Oscillations are widely distributed throughout the nervous system. A number of models accounting for their generation and their contribution to the synchronization of the concerned neurons, have been proposed. Most of these schemes involve inhibitory interneurons. Here we studied, in vivo, the firing patterns of interneurons, identified as presynaptic to the goldfish Mauthner (M) cell, and called passive hyperpolarizing potential (PHP) cells. We found that a subset of these interneurons was characterized by the presence of subthreshold oscillations of their membrane potential. Such oscillations near the firing threshold generated action potentials that were phased-locked on the oscillations and consequently, the distributions of time intervals between these spikes were observed at integral multiple values of the oscillation cycles. Two superimposed oscillatory processes have been identified. The amplitude of the first one, “the carrier,” was voltage dependent while that of the second, the “modulator,” was not. The frequency of the carrier was distributed among four values (140, 100, 71 or 50 Hz), the frequency of the “modulator” was about 50 Hz in almost all the investigated neurons. The demonstration that the 50 Hz oscillations were shared by almost all PHP exhibiting neurons strongly supports the notion that these cells act synchronously. Finally, auditory stimulations activated “silent” interneurons whereas they inhibited “active” ones, confirming that the presence of oscillations endows the M-cell inhibitory network with dynamic properties which can effectively organize the timing of motor behavior. Our results demonstrate that multiple frequencies, all in the gamma range, can coexist in the same network and that oscillations are present in a well defined population of inhibitory cells that controls fast decision-making.