Intrinsic firing properties in the avian auditory brain stem allow both integration and encoding of temporally modulated noisy inputs in vitro

Abstract

The intrinsic properties of tonically firing neurons in the cochlear nucleus contribute to representing average sound intensity by favoring synaptic integration across auditory nerve inputs, reducing phase locking to fine temporal acoustic structure and enhancing envelope locking. To determine whether tonically firing neurons of the avian cochlear nucleus angularis (NA) resemble ideal integrators, we investigated their firing responses to noisy current injections during whole cell patch-clamp recordings in brain slices. One subclass of neurons (36% of tonically firing neurons, mainly subtype tonic III) showed no significant changes in firing rate with noise fluctuations, acting like pure integrators. In contrast, many tonically firing neurons (>60%, mainly subtype tonic I or II) showed a robust sensitivity to noisy current fluctuations, increasing their firing rates with increased fluctuation amplitudes. For noise-sensitive tonic neurons, the firing rate vs. average current curves with noise had larger maximal firing rates, lower gains, and wider dynamic ranges compared with FI curves for current steps without noise. All NA neurons showed fluctuation-driven patterning of spikes with a high degree of temporal reliability and millisecond spike time precision. Single-spiking neurons in NA also responded to noisy currents with higher firing rates and reliable spike trains, although less precisely than nucleus magnocellularis neurons. Thus some NA neurons function as integrators by encoding average input levels over wide dynamic ranges regardless of current fluctuations, others detect the degree of coherence in the inputs, and most encode the temporal patterns contained in their inputs with a high degree of precision.