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Tuning to Binaural Cues in Human Auditory Cortex

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Abstract

Interaural level and time differences (ILD and ITD), the primary binaural cues for sound localization in azimuth, are known to modulate the tuned responses of neurons in mammalian auditory cortex (AC). The majority of these neurons respond best to cue values that favor the contralateral ear, such that contralateral bias is evident in the overall population response and thereby expected in population-level functional imaging data. Human neuroimaging studies, however, have not consistently found contralaterally biased binaural response patterns. Here, we used functional magnetic resonance imaging (fMRI) to parametrically measure ILD and ITD tuning in human AC. For ILD, contralateral tuning was observed, using both univariate and multivoxel analyses, in posterior superior temporal gyrus (pSTG) in both hemispheres. Response-ILD functions were U-shaped, revealing responsiveness to both contralateral and—to a lesser degree—ipsilateral ILD values, consistent with rate coding by unequal populations of contralaterally and ipsilaterally tuned neurons. In contrast, for ITD, univariate analyses showed modest contralateral tuning only in left pSTG, characterized by a monotonic response-ITD function. A multivoxel classifier, however, revealed ITD coding in both hemispheres. Although sensitivity to ILD and ITD was distributed in similar AC regions, the differently shaped response functions and different response patterns across hemispheres suggest that basic ILD and ITD processes are not fully integrated in human AC. The results support opponent-channel theories of ILD but not necessarily ITD coding, the latter of which may involve multiple types of representation that differ across hemispheres.

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Notes

  1. Note that sensitivity to ILD reflects both the influence of binaural sensitivity per se (Salminen 2015), including binaural interactions such as ipsilateral inhibition (Krumbholz et al. 2005b; Kitzes 2008; Stecker et al. 2015), and monaural intensity cues.

  2. A scree test was used to select the number of retained components; in most cases, less than 10 % decrease in residual pattern variance was noted beyond the 8th component.

  3. Given the nature of the stimulus employed (100-Hz broadband noise-burst trains), this distribution of ITD-independent activity appears consistent with past studies demonstrating sensitivity to stimulus periodicity in lateral HG (Griffiths et al. 1998, 2001; Patterson et al. 2002; Hall et al. 2005).

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Acknowledgments

The authors thank Jeff Stevenson, Baochang Chu, and Ken Maravilla for assistance with fMRI data collection; Andrew Brown and Geoff Boynton for helpful comments during the design phase; Jacqueline Bibee for assistance with signal denoising; and three anonymous reviewers for helpful comments on earlier versions of the manuscript. This work was supported by National Institutes of Health—National Institute on Deafness and Other Communication Disorders (NIDCD: R03-DC009482-02S1, T32-DC005361, and R01-DC011548). The content is solely the responsibility of the authors and does not represent the official views of the NSF, NIDCD, or the National Institutes of Health. Portions of this work appeared in the first author’s Ph.D. dissertation (McLaughlin 2013).

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McLaughlin, S.A., Higgins, N.C. & Stecker, G.C. Tuning to Binaural Cues in Human Auditory Cortex. JARO 17, 37–53 (2016). https://doi.org/10.1007/s10162-015-0546-4

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