Gap junction mediated feed-forward inhibition ensures ultra precise temporal patterning in vocal behavior

Abstract

Precise neuronal firing is especially important for behaviors highly dependent on the correct sequencing and timing of muscle activity patterns, such as acoustic signalling. We show that extreme temporal precision in motoneuronal firing within a hindbrain network that directly determines call duration, pulse repetition rate and fundamental frequency in a teleost fish, the Gulf toadfish, depends on gap junction-mediated, feed-forward glycinergic inhibition that generates a period of reduced probability of motoneuron activation. Super-resolution microscopy confirms glycinergic release sites contacting motoneuron somata and dendrites. Synchronous motoneuron activity can also induce action potential firing in pre-motoneurons, a feature that could figure prominently into motor timing. Gap junction-mediated, feed-forward glycinergic inhibition provides a novel means for achieving temporal precision in the millisecond range for rapid modulation of an acoustic signal and perhaps other motor behaviors.