Human auditory cortex is sensitive to the perceived clarity of speech

NeuroImage

Volumn 60, Issue 2, 2012, Pages 1490-1502

  Wild, Conor J ^a   Davis, Matthew H ^b   Johnsrude, Ingrid S ^a,c,d  

^a QUEEN S UNIVERSITY   (Canada)

^b MRC COGNITION AND BRAIN SCIENCES UNIT   (United Kingdom)

^c LINKÖPING UNIVERSITY   (Sweden)

^d QUEEN S UNIVERSITY   (Canada)

Author keywords

Feedback connections; FMRI; Inferior frontal gyrus; Predictive coding; Premotor cortex; Primary auditory cortex; Speech perception; Superior temporal sulcus; Top down influences

Indexed keywords

ADULT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUDITORY SYSTEM; BRAIN CORTEX; CONTROLLED STUDY; FEMALE; FRONTAL LOBE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; MOTOR CORTEX; NEUROIMAGING; NORMAL HUMAN; PILOT STUDY; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; SENSORY STIMULATION; SPEECH ANALYSIS; SPEECH PERCEPTION; TEMPORAL LOBE;

ADOLESCENT; ADULT; AUDITORY CORTEX; FEMALE; HUMANS; MALE; SPEECH; SPEECH PERCEPTION; YOUNG ADULT;

EID: 84857128343     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.01.035     Document Type: Article

References (104)

1. Abrams D.A., Nicol T., Zecker S., Kraus N. Right-hemisphere auditory cortex is dominant for coding syllable patterns in speech. J. Neurosci. 2008, 28:3958-3965.
2. Alink A., Schwiedrzik C.M., Kohler A., Singer W., Muckli L. Stimulus predictability reduces responses in primary visual cortex. J. Neurosci. 2010, 30:2960-2966.
3. Benoit C., Mohamadi T., Kandel S. Effects of phonetic context on audio-visual intelligibility of French. J. Speech Hear. Res. 1994, 37:1195-1203.
4. Bernstein L.E., Auer E.T., Moore J.K., Ponton C.W., Don M., Singh M. Visual speech perception without primary auditory cortex activation. Neuroreport 2002, 13:311.
5. Binder J.R., Frost J.A., Hammeke T.A., Rao S.M., Cox R.W. Function of the left planum temporale in auditory and linguistic processing. Brain 1996, 119:1239-1247.
6. Bizley J.K., Nodal F.R., Bajo V.M., Nelken I., King A.J. Physiological and anatomical evidence for multisensory interactions in auditory cortex. Cereb. Cortex 2007, 17:2172-2189.
7. Brett M., Anton J.-L., Valabregue R., Poline J.-B. Region of interest analysis using an SPM toolbox [abstract]. Presented at the 8th International Conference on Functional Mapping of the Human Brain, June 2-6, 2002, Sendai, Japan 2002.
8. Brosch M., Selezneva E., Scheich H. Nonauditory events of a behavioral procedure activate auditory cortex of highly trained monkeys. J. Neurosci. 2005, 25:6797-6806.
9. Calvert G.A. Activation of auditory cortex during silent lipreading. Science 1997, 276:593-596.
10. Cameron E.L., Tai J.C., Carrasco M. Covert attention affects the psychometric function of contrast sensitivity. Vis. Res. 2002, 42:949-967.
11. Carrasco M. Cross-modal attention enhances perceived contrast. Proc. Natl. Acad. Sci. 2009, 106:22039.
12. Carrasco M., Penpeci-Talgar C., Eckstein M. Spatial covert attention increases contrast sensitivity across the CSF: support for signal enhancement. Vis. Res. 2000, 40:1203-1215.
13. Cohen L., Lehéricy S., Chochon F., Lemer C., Rivaud S., Dehaene S. Language-specific tuning of visual cortex? Functional properties of the visual word form area. Brain 2002, 125:1054-1069.
14. Davis M.H., Johnsrude I.S. Hierarchical processing in spoken language comprehension. J. Neurosci. 2003, 23:3423.
15. Davis M.H., Johnsrude I.S., Hervais-Adelman A., Taylor K., McGettigan C. Lexical information drives perceptual learning of distorted speech: evidence from the comprehension of noise-vocoded sentences. J. Exp. Psychol. Gen. 2005, 134:222-241.
16. de la Mothe L.A., Blumell S., Kajikawa Y., Hackett T.A. Cortical connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J. Comp. Neurol. 2006, 496:27-71.
17. Devlin J.T., Raley J., Tunbridge E., Lanary K., Floyer-Lea A., Narain C., Cohen I., Behrens T., Jezzard P., Matthews P.M., Moore D.R. Functional asymmetry for auditory processing in human primary auditory cortex. J. Neurosci. 2003, 23:11516-11522.
18. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005, 25:1325-1335.
19. Falchier A., Clavagnier S., Barone P., Kennedy H. Anatomical evidence of multimodal integration in primate striate cortex. J. Neurosci. 2002, 22:5749-5759.
20. Fox M.D., Zhang D., Snyder A.Z., Raichle M.E. The global signal and observed anticorrelated resting state brain networks. J. Neurophysiol. 2009, 101:3270-3283.
21. Friston K. A theory of cortical responses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2005, 360:815-836.
22. Friston K.J., Williams S., Howard R., Frackowiak R.S., Turner R., et al. Movement-related effects in fMRI time-series. Magn. Reson. Med. 1996, 35:346-355.
23. Friston K.J., Harrison L., Penny W. Dynamic causal modelling. Neuroimage 2003, 19:1273-1302.
24. Friston K.J., Daunizeau J., Kilner J., Kiebel S.J. Action and behavior: a free-energy formulation. Biol. Cybern. 2010, 102:227-260.
25. Frost R. Toward a strong phonological theory of visual word recognition: true issues and false trails. Psychol. Bull. 1998, 123:71-99.
26. Fu K.-M.G., Johnston T.A., Shah A.S., Arnold L., Smiley J., Hackett T.A., Garraghty P.E., Schroeder C.E. Auditory cortical neurons respond to somatosensory stimulation. J. Neurosci. 2003, 23:7510-7515.
27. Fu K.-M.G., Shah A.S., O'Connell M.N., McGinnis T., Eckholdt H., Lakatos P., Smiley J., Schroeder C.E. Timing and laminar profile of eye-position effects on auditory responses in primate auditory cortex. J. Neurophysiol. 2004, 92:3522-3531.
28. Geschwind N., Levitsky W. Human brain: left-right asymmetries in temporal speech region. Science 1968, 161:186-187.
29. Ghazanfar A.A., Maier J.X., Hoffman K.L., Logothetis N.K. Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. J. Neurosci. 2005, 25:5004-5012.
30. Giraud A.L., Kell C., Thierfelder C., Sterzer P., Russ M.O., Preibisch C., Kleinschmidt A. Contributions of sensory input, auditory search and verbal comprehension to cortical activity during speech processing. Cereb. Cortex 2004, 14:247.
31. Gow D.W., Segawa J.A. Articulatory mediation of speech perception: a causal analysis of multi-modal imaging data. Cognition 2009, 110:222-236.
32. Greenwood D.D. A cochlear frequency-position function for several species-29years later. J. Acoust. Soc. Am. 1990, 87:2592-2605.
33. Hackett T.A. Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. J. Comp. Neurol. 2001, 441:197-222.
34. Hackett T.A. Multisensory convergence in auditory cortex, II. Thalamocortical connections of the caudal superior temporal plane. J. Comp. Neurol. 2007, 502:924-952.
35. Hackett T.A., Stepniewska I., Kaas J.H. Prefrontal connections of the parabelt auditory cortex in macaque monkeys. Brain Res. 1999, 817:45-58.
36. Hackett T.A., Preuss T.M., Kaas J.H. Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. The Journal of Comparative Neurology 2001, 441:197-222.
37. Hall D.A., Haggard M.P., Akeroyd M.A., Palmer A.R., Summerfield A.Q., Elliott M.R., Gurney E.M., Bowtell R.W. "Sparse" temporal sampling in auditory fMRI. Hum. Brain Mapp. 1999, 7:213-223.
38. Heinze H.J., Mangun G.R., Burchert W., Hinrichs H., Scholz M., Münte T.F., Gös A., Scherg M., Johannes S., Hundeshagen H., Gazzaniga M.S., Hillyard S.A. Combined spatial and temporal imaging of brain activity during visual selective attention in humans. Nature 1994, 372:543-546.
39. Hervais-Adelman A., Davis M.H., Johnsrude I.S., Carlyon R.P. Perceptual learning of noise vocoded words: effects of feedback and lexicality. J. Exp. Psychol. 2008, 34:460-474.
40. Hervais-Adelman, A., Carlyon, R.P., Johnsrude, I.S., Davis, M.H., 2010. Motor regions are recruited for effortful comprehension of noise-vocoded words: evidence from fMRI.
41. Hesselmann G., Sadaghiani S., Friston K.J., Kleinschmidt A. Predictive coding or evidence accumulation? False inference and neuronal fluctuations. PLoS One 2010, 5:e9926.
42. Iacoboni M. The role of premotor cortex in speech perception: evidence from fMRI and rTMS. J. Physiol. Paris 2008, 102:31-34.
43. Johnson J.A., Zatorre R.J. Attention to simultaneous unrelated auditory and visual events: behavioral and neural correlates. Cereb. Cortex 2005, 15:1609-1620.
44. Johnson J.A., Zatorre R.J. Neural substrates for dividing and focusing attention between simultaneous auditory and visual events. Neuroimage 2006, 31:1673-1681.
45. Kaas J.H., Hackett T.A. Subdivisions of auditory cortex and processing streams in primates. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11793.
46. Kalikow D.N., Stevens K.N., Elliott L.L. Development of a test of speech intelligibility in noise using sentence materials with controlled word predictability. J. Acoust. Soc. Am. 1977, 61:1337-1351.
47. Kayser C., Petkov C., Augath M., Logothetis N.K. Integration of touch and sound in auditory cortex. Neuron 2005, 48:373-384.
48. Kayser C., Petkov C., Augath M., Logothetis N.K. Functional imaging reveals visual modulation of specific fields in auditory cortex. J. Neurosci. 2007, 27:1824-1835.
49. Koch M.A., Norris D.G., Hund-Georgiadis M. An investigation of functional and anatomical connectivity using magnetic resonance imaging. Neuroimage 2002, 16:241-250.
50. Lakatos P., Chen C.-M., O'Connell M.N., Mills A., Schroeder C.E. Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 2007, 53:279-292.
51. Lehmann C., Herdener M., Esposito F., Hubl D., di Salle F., Scheffler K., Bach D.R., Federspiel A., Kretz R., Dierks T., Seifritz E. Differential patterns of multisensory interactions in core and belt areas of human auditory cortex. Neuroimage 2006, 31:294-300.
52. Loftus G., Masson M. Using confidence-intervals in within-subject designs. Psychon. Bull. Rev. 1994, 1:476-490.
53. Macey P.M., Macey K.E., Kumar R., Harper R.M. A method for removal of global effects from fMRI time series. Neuroimage 2004, 22:360-366.
54. Macleod A., Summerfield Q. Quantifying the contribution of vision to speech perception in noise. Br. J. Audiol. 1987, 21:131-141.
55. Martuzzi R., Murray M.M., Michel C.M., Thiran J.-P., Maeder P.P., Clarke S., Meuli R.A. Multisensory interactions within human primary cortices revealed by BOLD dynamics. Cereb. Cortex 2007, 17:1672-1679.
56. Miller G.A., Isard S. Some perceptual consequences of linguistic rules. J. Verbal Learn. Verbal Behav. 1963, 2:217-228.
57. Miller G.A., Heise G.A., Lichten W. The intelligibility of speech as a function of the context of the test materials. J. Exp. Psychol. 1951, 41:329-335.
58. Morosan P., Rademacher J., Schleicher A., Amunts K., Schormann T., Zilles K. Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage 2001, 13:684-701.
59. Mumford D. On the computational architecture of the neocortex. Biol. Cybern. 1992, 66:241-251.
60. Murray S.O., Kersten D., Olshausen B.A., Schrater P., Woods D.L. Shape perception reduces activity in human primary visual cortex. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15164.
61. Murray S.O., Schrater P., Kersten D. Perceptual grouping and the interactions between visual cortical areas. Neural Netw. 2004, 17:695-705.
62. Norris D. Shortlist: a connectionist model of continuous speech recognition. Cognition 1994, 52:189-234.
63. Norris D., McQueen J.M. Shortlist B: a Bayesian model of continuous speech recognition. Psychol. Rev. 2008, 115:357-395.
64. Norris D., McQueen J.M., Cutler A. Merging information in speech recognition: feedback is never necessary. Behav. Brain Sci. 2000, 23. 299-+.
65. Nygaard L., Pisoni D. Talker-specific learning in speech perception. Percept. Psychophys. 1998, 60:355-376.
66. Orden G.C. A ROWS is a ROSE: spelling, sound, and reading. Mem. Cogn. 1987, 15:181-198.
67. Osnes B., Hugdahl K., Specht K. Effective connectivity analysis demonstrates involvement of premotor cortex during speech perception. NeuroImage 2011, 54:2437-2445.
68. Pandya D.N., Hallett M., Mukherjee S.K. Intra-and interhemispheric connections of the neocortical auditory system in the rhesus monkey. Brain Research 1969, 14:49-65.
69. Pekkola J., Ojanen V., Autti T., Jääskeläinen I.P., Möttönen R., Tarkiainen A., Sams M. Primary auditory cortex activation by visual speech: an fMRI study at 3T. Neuroreport 2005, 16:125.
70. Penhune V.B., Zatorre R.J., MacDonald J.D., Evans A.C. Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb. Cortex 1996, 6:661.
71. Pestilli F., Carrasco M. Attention enhances contrast sensitivity at cued and impairs it at uncued locations. Vis. Res. 2005, 45:1867-1875.
72. Petkov C.I., Kang X., Alho K., Bertrand O., Yund E.W., Woods D.L. Attentional modulation of human auditory cortex. Nat. Neurosci. 2004, 7:658-663.
73. Pugh K.R., Shaywitz B.A., Shaywitz S.E., Constable R.T., Skudlarski P., Fulbright R.K., Bronen R.A., Shankweiler D.P., Katz L., Fletcher J.M., Gore J.C. Cerebral organization of component processes in reading. Brain 1996, 119:1221-1238.
74. Rao R.P.N., Ballard D.H. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 1999, 2:79.
75. Rastle K., Brysbaert M. Masked phonological priming effects in English: are they real? Do they matter?. Cogn. Psychol. 2006, 53:97-145.
76. Ratcliff G., Dila C., Taylor L., Milner B. The morphological asymmetry of the hemispheres and cerebral dominance for speech: a possible relationship. Brain Lang. 1980, 11:87-98.
77. Rissman J., Gazzaley A., D'Esposito M. Measuring functional connectivity during distinct stages of a cognitive task. Neuroimage 2004, 23:752-763.
78. Rockland K.S., Ojima H. Multisensory convergence in calcarine visual areas in macaque monkey. Int. J. Psychophysiol. 2003, 50:19-26.
79. Rodd J.M., Davis M.H., Johnsrude I.S. The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. Cereb. Cortex 2005, 15:1261.
80. Romanski L.M., Bates J.F., Goldman-Rakic P.S. Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J. Comp. Neurol. 1999, 403:141-157.
81. Romanski L.M., Tian B., Fritz J., Mishkin M., Goldman-Rakic P.S., Rauschecker J.P. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat. Neurosci. 1999, 2:1131-1136.
82. Sams M., Aulanko R., Hämäläinen M., Hari R., Lounasmaa O.V., Lu S.-T., Simola J. Seeing speech: visual information from lip movements modifies activity in the human auditory cortex. Neurosci. Lett. 1991, 127:141-145.
83. Schroeder C.E., Foxe J.J. The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. Cogn. Brain Res. 2002, 14:187-198.
84. Schroeder C.E., Lindsley R.W., Specht C., Marcovici A., Smiley J.F., Javitt D.C. Somatosensory input to auditory association cortex in the macaque monkey. J. Neurophysiol. 2001, 85:1322-1327.
85. Shannon R.V., Zeng F.G., Kamath V., Wygonski J., Ekelid M. Speech recognition with primarily temporal cues. Science 1995, 270:303-304.
86. Shattuck D.W., Mirza M., Adisetiyo V., Hojatkashani C., Salamon G., Narr K.L., Poldrack R.A., Bilder R.M., Toga A.W. Construction of a 3D probabilistic atlas of human cortical structures. Neuroimage 2008, 39:1064-1080.
87. Smiley J.F., Falchier A. Multisensory connections of monkey auditory cerebral cortex. Hear. Res. 2009, 258:37-46.
88. Sumby W.H., Pollack I. Visual contribution to speech intelligibility in noise. J. Acoust. Soc. Am. 1954, 26:212-215.
89. Summerfield C., Koechlin E. A neural representation of prior information during perceptual inference. Neuron 2008, 59:336-347.
90. Tahmasebi A., Abolmaesumi P., Geng X., Morosan P., Amunts K., Christensen G., Johnsrude I. A new approach for creating customizable cytoarchitectonic probabilistic maps without a template. Med. Image Comput. Comput.-Assist. Interv.-MICCAI 2009, 795-802.
91. Thompson-Schill S.L., D'Esposito M., Aguirre G.K., Farah M.J. Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:14792.
92. Treue S. Perceptual enhancement of contrast by attention. Trends Cogn. Sci. 2004, 8:435-437.
93. van Atteveldt N., Formisano E., Goebel R., Blomert L. Integration of letters and speech sounds in the human brain. Neuron 2004, 43:271-282.
94. van Atteveldt N., Formisano E., Blomert L., Goebel R. The effect of temporal asynchrony on the multisensory integration of letters and speech sounds. Cereb. Cortex 2007, 17:962-974.
95. van Wassenhove V., Grant K.W., Poeppel D. Visual speech speeds up the neural processing of auditory speech. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1181-1186.
96. van Wassenhove V., Grant K.W., Poeppel D. Temporal window of integration in auditory-visual speech perception. Neuropsychologia 2007, 45:598-607.
97. Vinckier F., Dehaene S., Jobert A., Dubus J., Sigman M., Cohen L. Hierarchical coding of letter strings in the ventral stream: dissecting the inner organization of the visual word-form system. Neuron 2007, 55:143-156.
98. Wagner A.D., Paré-Blagoev E.J., Clark J., Poldrack R.A. Recovering meaning: left prefrontal cortex guides controlled semantic retrieval. Neuron 2001, 31:329-338.
99. Werner-Reiss U., Kelly K.A., Trause A.S., Underhill A.M., Groh J.M. Eye position affects activity in primary auditory cortex of primates. Curr. Biol. 2003, 13:554-562.
100. Wilson S.M., Iacoboni M. Neural responses to non-native phonemes varying in producibility: evidence for the sensorimotor nature of speech perception. Neuroimage 2006, 33:316-325.
101. Wilson S.M., Saygin A.P., Sereno M.I., Iacoboni M. Listening to speech activates motor areas involved in speech production. Nat. Neurosci. 2004, 7:701-702.
102. Winer J.A. Decoding the auditory corticofugal systems. Hear. Res. 2005, 207:1-9.
103. Zatorre R.J., Belin P., Penhune V.B. Structure and function of auditory cortex: music and speech. Trends Cogn. Sci. 2002, 6:37-46.
104. Zekveld A.A., Kramer S.E., Kessens J.M., Vlaming M.S.M.G., Houtgast T. The benefit obtained from visually displayed text from an automatic speech recognizer during listening to speech presented in noise. Ear Hear. 2008, 29:838-852.