Distinct cell classes in the superior paraolivary nucleus (SPN) region in the gerbil auditory brainstem revealed by in vivo physiological and anatomical characterization

Abstract

The superior para-olivary nucleus (SPN or SPON) is a prominent nucleus in the superior olivary complex of the auditory brainstem. The cellular composition of the nucleus reportedly differs between species, but a prominent recurring feature is the unusual characteristic to not respond during a sound but at its offset. Blocking glycine has shown that sound-induced inhibition is the mechanism, but the time course of the responsible synaptic events has not been directly measured in vivo. We obtained intracellular recordings in the Mongolian gerbil (meriones unguiculatus) with patch electrodes containing biocytin, and retrieved 12 labeled neurons with large dendritic trees within and around the SPN region. We found that these neurons could be categorized into three classes that show consistency along multiple dimensions like ultrastructure, spontaneous activity, and responses to current injection and a variety of ipsi- and contralateral sounds. Fast cells fire at onset of depolarizing current, generate short-latency rebound spikes to sound or hyperpolarizing current, and show dense synaptic coverage. Slow cells show sparse synaptic coverage, sustained responses to depolarization, and inhibition with a slow time course to hyperpolarizing current or sound. Uninhibited cells form a third class which profoundly differ in their responses to sound, lacking rebound spiking. We propose that fast cells project to the inferior colliculus, and slow cells to the cochlear nucleus.