Tuning to Binaural Cues in Human Auditory Cortex
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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.
Keywordsauditory space fMRI ILD ITD hemispheric asymmetry interaural differences
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).
Conflict of Interest
The authors declare that they have no conflict of interest.
- Ahveninen J, Jääskeläinen IP, Raij T, Bonmassar G, Devore S, Hämäläinen M, Levänen S, Lin F-H, Sams M, Shinn-Cunningham BG, Witzel T, Belliveau JW (2006) Task-modulated “what” and “where” pathways in human auditory cortex. Proc Natl Acad Sci U S A 103(39):14608–14613PubMedCentralCrossRefPubMedGoogle Scholar
- Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57(1):289–300Google Scholar
- Blauert J (1983) Spatial hearing. MIT Press, CambridgeGoogle Scholar
- Boester L (1994) Binaural time and intensity discrimination following unilateral auditory cortex ablation in Japanese macaques (Macaca fuscata). Master’s thesis, University of Toledo, ToledoGoogle Scholar
- Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31(3):968–980CrossRefPubMedGoogle Scholar
- Kelly RE Jr, Alexopoulos GS, Wang Z, Gunning FM, Murphy CF, Morimoto SS, Kanellopoulos D, Jia Z, Lim KO, Hoptman MJ (2010) Visual inspection of independent components: defining a procedure for artifact removal from fMRI data. J Neurosci Methods 189(2):233–245PubMedCentralCrossRefPubMedGoogle Scholar
- Kuhn G (1977) Model for interaural time differences in the azimuthal plane. J Acoust Soc Am 62(157–67)Google Scholar
- McLaughlin SA (2013) Functional magnetic resonance imaging of human auditory cortical tuning to interaural level and time differences. PhD thesis, University of WashingtonGoogle Scholar
- Palmer A, Kuwada S (2005) Binaural and spatial coding in the inferior colliculus. In: Winer JA, S. C. (eds) The inferior colliculus. Springer, New York, chapter 13, 377–410Google Scholar
- Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219CrossRefPubMedGoogle Scholar
- Stecker GC (2010) More modeling of temporal weighting functions for interaural time and level differences. Assoc Res Otolaryngol Abs 33:831Google Scholar
- Stecker GC, McLaughlin SA, Higgins NC (2015) Monaural and binaural contributions to interaural-level-difference sensitivity in human auditory cortex. NeuroimageGoogle Scholar
- Woldorff MG, Tempelmann C, Fell J, Tegeler C, Gaschler-Markefski B, Hinrichs H, Heinz HJ, Scheich H (1999) Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography. Hum Brain Mapp 7(1):49–66CrossRefPubMedGoogle Scholar