Structures, Mechanisms, and Energetics in Temporal Processing

Abstract

The ability of mammals to discriminate which ear is the first to receive acoustic stimuli with a resolution of approximately 10 μS is remarkable. It requires precise detection of the acoustic signal by the inner ear and equally precise communication and refinement of the information through at least three synapses prior to dichotic integration in the superior olive. The Jeffress place theory for sound localization was introduced in 1948 and remains a touchstone for research in the area. At its heart are assumptions about the ability of the auditory system to detect, transmit, and process temporal information. More than a half century of research has established that rapid processing of acoustic information in hair cells and brain stem auditory neurons is achieved with surprisingly similar mechanisms having high metabolic demands. Short electrical time constants are required for rapid temporal processing. Hair cells and auditory brain stem neurons have a high conductance at their resting potential that contributes to short time constants, but at the same time leads to large resting currents that have high metabolic demands. The membrane proteins that modulate these currents have a shallow, nonuniform, voltage dependence that results in a broad dynamic range, and further increases metabolic demand. High-speed performance is energetically costly, as is the case with automobiles, and provides the rationale for the high metabolic activity associated with auditory structures. Energetic considerations provide a conceptual bridge between the peripheral and brain stem auditory system.