Hemispheric and Sex Differences in Mustached Bat Primary Auditory Cortex Revealed by Neural Responses to Slow Frequency Modulations.

Stuart D. Washington,Georgios A. Keliris,Jagmeet S. Kanwal,Dominique L. Pritchett

doi:10.3390/sym13061037

Abstract

The mustached bat (Pteronotus parnellii) is a mammalian model of cortical hemispheric asymmetry. In this species, complex social vocalizations are processed preferentially in the left Doppler-shifted constant frequency (DSCF) subregion of primary auditory cortex. Like hemispheric specializations for speech and music, this bat brain asymmetry differs between sexes (i.e., males>females) and is linked to spectrotemporal processing based on selectivities to frequency modulations (FMs) with rapid rates (>0.5 kHz/ms). Analyzing responses to the long-duration (>10 ms), slow-rate (<0.5 kHz/ms) FMs to which most DSCF neurons respond may reveal additional neural substrates underlying this asymmetry. Here, we bilaterally recorded responses from 176 DSCF neurons in male and female bats that were elicited by upward and downward FMs fixed at 0.04 kHz/ms and presented at 0-90 dB SPL. In females, we found inter-hemispheric latency differences consistent with applying different temporal windows to precisely integrate spectrotemporal information. In males, we found a substrate for asymmetry less related to spectrotemporal processing than to acoustic energy (i.e., amplitude). These results suggest that in the DSCF area, (1) hemispheric differences in spectrotemporal processing manifest differently between sexes, and (2) cortical asymmetry for social communication is driven by spectrotemporal processing differences and neural selectivities for amplitude.

Highlights

A left-hemispheric advantage for receptive language in general and especially speech perception [1,2] is characteristic of the human auditory cortex
To understand the neuro-acoustic basis of this finding, we investigated how Doppler-shifted constant frequency (DSCF) neural selectivities for CFs and linear frequency modulations (FMs) differ between hemispheres, taking into account the sex differences commonly observed in hemispheric asymmetries in songbirds, rodents, and humans [67]
We organized our data into four groups (Left Male, Right Male, Left Female, and Right Female) to test a prior hypothesis based on the sex-dependent asymmetries and combined these groups whenever the need to test other related hypotheses arose

Summary

Introduction

A left-hemispheric advantage for receptive language in general and especially speech perception [1,2] is characteristic of the human auditory cortex. Numerous studies of healthy [3,4,5,6,7,8,9] and clinical [10,11,12,13,14,15] human populations report that the left auditory cortex (AC) displays high temporal resolution relative to the right This enhanced temporal resolution enables left AC to better process speech sounds containing rapid formant transitions, which are comparable to frequency modulations (FMs) [16,17]. Multiple domain-general hypotheses [28,29] attribute these findings to the acoustic uncertainty principle, which states that there is an inverse relationship between temporal and spectral resolution governed by the same mathematics underlying Heisenberg’s quantum uncertainty principle [30,31].

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Conclusion