Serial and parallel processing in primate auditory cortex: a comparison of response properties in the core, belt, and parabelt

Abstract

Audition is critical for communication and survival, yet the cortical pathways and mechanisms by which complex sounds are processed remain poorly understood. From the results of a number of studies, a working model of primate auditory cortex has emerged, where it is proposed to contain three regions: core, belt, and parabelt. These three regions can be thought of as levels of processing, and are subdivided into multiple areas, distinguished by unique anatomical and physiological profiles. Anatomical connections between regions and areas have suggested a hierarchy of processing, but the direction and flow of information within and between regions and areas remains an active area of study. Here, we characterize the response properties of neurons in a number of areas across all three regions of the auditory cortex of awake macaques. We find that response latencies are consistent with the flow of information in two directions: across regional level (core-belt-parabelt) and across areas in a caudal to rostral direction. Evidence from response tuning to temporally modulated frequencies also is consistent with a direction of flow across regional level. Though there is evidence of directional flow in multiple areas, it is clear that areas are responding within a very close timescale to each other. Lastly, an analysis of pairwise correlations within and across areas suggests auditory cortex is organized into a weakly yet isotopically connected functional network, where effective connectivity is stronger within an area than across areas. This series of studies is the most complete coverage of multiple areas in primate auditory cortex in the literature to date. Converging evidence from both physiology and anatomy points to an emerging understanding that primate auditory cortex processes sound in multiple areas with a strong degree of parallel processing. This is an architecture optimally designed for the processing of rapid time-based stimuli such as sound.