Electrophysiological correlates of divergent projections in the avian superior olivary nucleus

Abstract

The physiological diversity of inhibitory neurons provides ample opportunity to influence a wide range of computational roles through their varied activity patterns, especially via feedback loops. In the avian auditory brainstem, inhibition originates primarily from the superior olivary nucleus (SON) and so it is critical to understand the intrinsic physiological properties and processing capabilities of these neurons. Neurons in the SON receive ascending input via the cochlear nuclei: directly from the intensity-coding cochlear nucleus angularis (NA) and indirectly via the interaural timing nucleus laminaris (NL), which itself receives input from cochlear nucleus magnocellularis. Two distinct populations of SON neurons provide either inhibitory feedback to ipsilateral NA, NL, and the timing cochlear nucleus NM, or to the contralateral SON. To determine whether these populations correspond to distinct response types, we investigated their electrophysiology in brain stem slices using patch clamp electrophysiology. We identified three phenotypes: single-spiking, chattering tonic, and regular tonic neurons. The two tonic phenotypes displayed distinct firing patterns and different membrane properties. Additionally, fluctuating noisy currents were used to probe the capability of SON neurons to encode temporal features. Each of the three phenotypes had a distinct level of sensitivity to this temporally modulated input. By using cell fills and anatomical reconstructions, we could correlate the firing phenotypes with their axonal projection patterns. We found that SON axons exited via three fiber tracts with specific phenotypes comprising each tract. Two ipsilateral tracts exit the SON, with the laterally projecting tract composed entirely of regular tonic neurons and medially projecting tract composed of both regular and chattering tonic neurons. The contralateral projection was composed entirely of single spiking neurons. These results provide a basis for understanding the role of specific inhibitory cell types in auditory function and elucidate the organization of the SON outputs.