Evidence for Distinct Human Auditory Cortex Regions for Sound Location Versus Identity Processing

Overview

Journal Nat Commun

Specialty Biology

Date 2013 Oct 15

PMID 24121634

Citations 34

Authors

Jyrki Ahveninen

Samantha Huang

Aapo Nummenmaa

John W Belliveau

An-Yi Hung

Iiro P Jaaskelainen

Josef P Rauschecker

Stephanie Rossi

Hannu Tiitinen

Tommi Raij

Affiliations

Soon will be listed here.

Abstract

Neurophysiological animal models suggest that anterior auditory cortex (AC) areas process sound identity information, whereas posterior ACs specialize in sound location processing. In humans, inconsistent neuroimaging results and insufficient causal evidence have challenged the existence of such parallel AC organization. Here we transiently inhibit bilateral anterior or posterior AC areas using MRI-guided paired-pulse transcranial magnetic stimulation (TMS) while subjects listen to Reference/Probe sound pairs and perform either sound location or identity discrimination tasks. The targeting of TMS pulses, delivered 55-145 ms after Probes, is confirmed with individual-level cortical electric-field estimates. Our data show that TMS to posterior AC regions delays reaction times (RT) significantly more during sound location than identity discrimination, whereas TMS to anterior AC regions delays RTs significantly more during sound identity than location discrimination. This double dissociation provides direct causal support for parallel processing of sound identity features in anterior AC and sound location in posterior AC.

Citing Articles

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References

Thivard L, Belin P, Zilbovicius M, Poline J, Samson Y . A cortical region sensitive to auditory spectral motion. Neuroreport. 2000; 11(13):2969-72. DOI: 10.1097/00001756-200009110-00028. View

Pascual-Leone A, Walsh V, Rothwell J . Transcranial magnetic stimulation in cognitive neuroscience--virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol. 2001; 10(2):232-7. DOI: 10.1016/s0959-4388(00)00081-7. View

Hall D, Plack C . Pitch processing sites in the human auditory brain. Cereb Cortex. 2008; 19(3):576-85. PMC: 2638814. DOI: 10.1093/cercor/bhn108. View

Puschmann S, Uppenkamp S, Kollmeier B, Thiel C . Dichotic pitch activates pitch processing centre in Heschl's gyrus. Neuroimage. 2009; 49(2):1641-9. DOI: 10.1016/j.neuroimage.2009.09.045. View

Zatorre R, Evans A, Meyer E, Gjedde A . Lateralization of phonetic and pitch discrimination in speech processing. Science. 1992; 256(5058):846-9. DOI: 10.1126/science.1589767. View

Rossi S, Hallett M, Rossini P, Pascual-Leone A . Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 2009; 120(12):2008-2039. PMC: 3260536. DOI: 10.1016/j.clinph.2009.08.016. View

Nummenmaa A, Stenroos M, Ilmoniemi R, Okada Y, Hamalainen M, Raij T . Comparison of spherical and realistically shaped boundary element head models for transcranial magnetic stimulation navigation. Clin Neurophysiol. 2013; 124(10):1995-2007. PMC: 3790855. DOI: 10.1016/j.clinph.2013.04.019. View

Payne B, Lomber S . A method to assess the functional impact of cerebral connections on target populations of neurons. J Neurosci Methods. 1999; 86(2):195-208. DOI: 10.1016/s0165-0270(98)00166-6. View

Kujirai T, Caramia M, Rothwell J, Day B, Thompson P, Ferbert A . Corticocortical inhibition in human motor cortex. J Physiol. 1993; 471:501-19. PMC: 1143973. DOI: 10.1113/jphysiol.1993.sp019912. View

10.

Alain C, Arnott S, Hevenor S, Graham S, Grady C . "What" and "where" in the human auditory system. Proc Natl Acad Sci U S A. 2001; 98(21):12301-6. PMC: 59809. DOI: 10.1073/pnas.211209098. View

11.

Patterson R, Uppenkamp S, Johnsrude I, Griffiths T . The processing of temporal pitch and melody information in auditory cortex. Neuron. 2002; 36(4):767-76. DOI: 10.1016/s0896-6273(02)01060-7. View

12.

Tian B, Reser D, Durham A, Kustov A, Rauschecker J . Functional specialization in rhesus monkey auditory cortex. Science. 2001; 292(5515):290-3. DOI: 10.1126/science.1058911. View

13.

At A, Spierer L, Clarke S . The role of the right parietal cortex in sound localization: a chronometric single pulse transcranial magnetic stimulation study. Neuropsychologia. 2011; 49(9):2794-7. DOI: 10.1016/j.neuropsychologia.2011.05.024. View

14.

Wilke M, Kagan I, Andersen R . Functional imaging reveals rapid reorganization of cortical activity after parietal inactivation in monkeys. Proc Natl Acad Sci U S A. 2012; 109(21):8274-9. PMC: 3361455. DOI: 10.1073/pnas.1204789109. View

15.

Salminen N, May P, Alku P, Tiitinen H . A population rate code of auditory space in the human cortex. PLoS One. 2009; 4(10):e7600. PMC: 2762079. DOI: 10.1371/journal.pone.0007600. View

16.

Vanduffel W, Payne B, Lomber S, Orban G . Functional impact of cerebral connections. Proc Natl Acad Sci U S A. 1997; 94(14):7617-20. PMC: 23871. DOI: 10.1073/pnas.94.14.7617. View

17.

Romanski L, Tian B, Fritz J, Mishkin M, Goldman-Rakic P, Rauschecker J . Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci. 1999; 2(12):1131-6. PMC: 2778291. DOI: 10.1038/16056. View

18.

Rauschecker J, Scott S . Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci. 2009; 12(6):718-24. PMC: 2846110. DOI: 10.1038/nn.2331. View

19.

Clarey J, Tweedale R, Calford M . Interhemispheric modulation of somatosensory receptive fields: evidence for plasticity in primary somatosensory cortex. Cereb Cortex. 1996; 6(2):196-206. DOI: 10.1093/cercor/6.2.196. View

20.

Popelar J, Nwabueze-Ogbo F, Syka J . Changes in neuronal activity of the inferior colliculus in rat after temporal inactivation of the auditory cortex. Physiol Res. 2003; 52(5):615-28. View