Abstract

Based on anatomical connectivity and basic response characteristics, primate auditory cortex is divided into a central core surrounded by belt and parabelt regions. The encoding of pitch, a prototypical element of sound identity, has been studied in primary auditory cortex (A1) but little is known about how it is encoded and represented beyond A1. The caudal auditory belt and parabelt cortical fields process spatial information but also contain information on non-spatial aspects of sounds. In this study, we examined neuronal responses in these areas to pitch-varied marmoset vocalizations, to derive the consequent representation of pitch in these regions and the potential underlying mechanisms, to compare to the encoding and representation of pitch of the same sounds in A1. With respect to response patterns to the vocalizations, neurons in caudal medial belt (CM) showed similar short-latency and short-duration response patterns to A1, but caudal lateral belt (CL) neurons at the same hierarchical level and caudal parabelt (CPB) neurons at a higher hierarchical level showed delayed or much delayed response onset and prolonged response durations. With respect to encoding of pitch, neurons in all cortical fields showed sensitivity to variations in the vocalization pitch either through modulation of spike-count or of first spike-latency. The utility of the encoding mechanism differed between fields: pitch sensitivity was reliably represented by spike-count variations in A1 and CM, while first spike-latency variation was better for encoding pitch in CL and CPB. In summary, our data show that (a) the traditionally-defined belt area CM is functionally very similar to A1 with respect to the representation and encoding of complex naturalistic sounds, (b) the CL belt area, at the same hierarchical level as CM, and the CPB area, at a higher hierarchical level, have very different response patterns and appear to use different pitch-encoding mechanisms, and (c) caudal auditory fields, proposed to be specialized for encoding spatial location, can also contain robust representations of sound identity.

Highlights

  • Primate auditory cortex is classically divided into three major, putatively-sequential, hierarchical processing stages, the core, belt, and parabelt regions (Kaas and Hackett, 2000), each with multiple areas likely to have different functions (Tian et al, 2001; Bendor and Wang, 2008; Fukushima et al, 2014)

  • In this study we investigated the mechanisms for neuronal encoding of variations in the pitch of natural vocalizations in core (A1) and a set of caudal belt and caudal parabelt (CPB) auditory cortex fields

  • These fields differ in basic neuronal response characteristics including pure tone tuning bandwidths and temporal response features like latency and duration, as reported previously (Recanzone, 2000; Hackett, 2011)

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Summary

INTRODUCTION

Primate auditory cortex is classically divided into three major, putatively-sequential, hierarchical processing stages, the core, belt, and parabelt regions (Kaas and Hackett, 2000), each with multiple areas likely to have different functions (Tian et al, 2001; Bendor and Wang, 2008; Fukushima et al, 2014). In a recent study of marmoset A1 (Zhu et al, 2019), we found that the majority of neurons in the region of representation of high frequencies (high CF region) can encode the pitch of naturalistic vocalizations, suggesting that distributed activity across A1 can represent the pitch of natural sounds over a functionally-relevant range for differentiating individuals by their vocalizations (Weiss et al, 2001; Bezerra and Souto, 2008). We found that subpopulations of neurons in caudal auditory cortex exhibited both similarities and difference in temporal response patterns, compared to A1 neurons Neurons in both A1 and caudal areas are able to represent vocalization pitch changes via both response intensity (spike-count) and latency, with different populations showing different coding strategies

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