Speech-specific tuning of neurons in human superior temporal gyrus

Cerebral Cortex

Volumn 24, Issue 10, 2014, Pages 2679-2693

  Chan, Alexander M ^a,b   Dykstra, Andrew R ^a,b   Jayaram, Vinay ^c   Leonard, Matthew K ^d   Travis, Katherine E ^d   Gygi, Brian ^e   Baker, Janet M ^f   Eskandar, Emad ^b   Hochberg, Leigh R ^b   Halgren, Eric ^d   Cash, Sydney S ^b  

^a HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e The National Institute for Health Research Health Protection Research Unit in Blood Borne and Sexually Transmitted Infections at University College London in partnership with UK Health Security Agency   (United Kingdom)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Audition; Human single units; Microelectrodes; Speech perception; Superior temporal gyrus

Indexed keywords

ACTION POTENTIAL; ADULT; ARTICLE; CASE REPORT; CONTROLLED STUDY; CONVERSATION; DECISION MAKING; HUMAN; INTRACTABLE EPILEPSY; MALE; NERVE CELL; PHONEME; PRIORITY JOURNAL; PURE TONE AUDIOMETRY; READING; RECEPTIVE FIELD; SPEECH; SUPERIOR TEMPORAL GYRUS; AUDITORY STIMULATION; PHONETICS; PHYSIOLOGY; SPEECH PERCEPTION; TEMPORAL LOBE;

ACOUSTIC STIMULATION; ADULT; HUMANS; MALE; NEURONS; PHONETICS; SPEECH PERCEPTION; TEMPORAL LOBE;

EID: 84920569237     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bht127     Document Type: Article

References (87)

1. Arnott SR, Binns MA, Grady CL, Alain C. 2004. Assessing the auditory dual-pathway model in humans. NeuroImage. 22:401-408.
2. Attwell D, Laughlin SB. 2001. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab. 21:1133-1145.
3. Baess P, Horvath J, Jacobsen T, Schroger E. 2011. Selective suppression of self-initiated sounds in an auditory stream: an ERP study. Psychophysiology. 48:1276-1283.
4. Bartho P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsaki G. 2004. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol. 92:600-608.
5. Binder JR, Frost JA, Hammeke TA, Bellgowan PS, Springer JA, Kaufman JN, Possing ET. 2000. Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex. 10:512-528.
6. Binder JR, Liebenthal E, Possing ET, Medler DA, Ward BD. 2004. Neural correlates of sensory and decision processes in auditory object identification. Nat Neurosci. 7:295-301.
7. Binder JR, Medler DA, Westbury CF, Liebenthal E, Buchanan L. 2006. Tuning of the human left fusiform gyrus to sublexical orthographic structure. NeuroImage. 33:739-748.
8. Bitterman Y, Mukamel R, Malach R, Fried I, Nelken I. 2008. Ultra-fine frequency tuning revealed in single neurons of human auditory cortex. Nature. 451:197-201.
9. Boatman D, Lesser RP, Gordon B. 1995. Auditory speech processing in the left temporal lobe: an electrical interference study. Brain Lang. 51:269-290.
10. Braun M, Hutzler F, Ziegler JC, Dambacher M, Jacobs AM. 2009. Pseudohomophone effects provide evidence of early lexicophonological processing in visual word recognition. Hum Brain Mapp. 30:1977-1989.
11. Chan AM, Baker JM, Eskandar E, Schomer D, Ulbert I, Marinkovic K, Cash SS, Halgren E. 2011. First-pass selectivity for semantic categories in human anteroventral temporal lobe. J Neurosci. 31:18119-18129.
12. Chan AM, Halgren E, Marinkovic K, Cash SS. 2011. Decoding word and category-specific spatiotemporal representations from MEG and EEG. NeuroImage. 54:3028-3039.
13. Chang EF, Rieger JW, Johnson K, Berger MS, Barbaro NM, Knight RT. 2010. Categorical speech representation in human superior temporal gyrus. Nat Neurosci. 13:1428-1432.
14. Christoffels IK, Formisano E, Schiller NO. 2007. Neural correlates of verbal feedback processing: an fMRI study employing overt speech. Hum Brain Mapp. 28:868-879.
15. Coltheart M, Curtis B, Atkins P, Haller M. 1993. Models of reading aloud: dual-route and parallel-distributed-processing approaches. Vol. 100. Washington (DC): American Psychological Association.
16. Creutzfeldt O, Ojemann G, Lettich E. 1989a. Neuronal activity in the human lateral temporal lobe. I. Responses to speech. Exp Brain Res. 77:451-475.
17. Creutzfeldt O, Ojemann G, Lettich E. 1989b. Neuronal activity in the human lateral temporal lobe. II. Responses to the subjects own voice. Exp Brain Res. 77:476-489.
18. Crinion JT, Lambon-Ralph MA, Warburton EA, Howard D, Wise RJ. 2003. Temporal lobe regions engaged during normal speech comprehension. Brain. 126:1193-1201.
19. Crone NE, Boatman D, Gordon B, Hao L. 2001. Induced electrocorticographic gamma activity during auditory perception. Brazier Awardwinning article, 2001. Clin Neurophysiol. 112:565-582.
20. Curio G, Neuloh G, Numminen J, Jousmaki V, Hari R. 2000. Speaking modifies voice-evoked activity in the human auditory cortex. Hum Brain Mapp. 9:183-191.
21. Dale AM, Liu AK, Fischl BR, Buckner RL, Belliveau JW, Lewine JD, Halgren E. 2000. Dynamic statistical parametric mapping: combining fMRI and MEG for high-resolution imaging of cortical activity. Neuron. 26:55-67.
22. Davis S, Mermelstein P. 1980. Comparison of parametric representations for monosyllabic word recognition in continuously spoken sentences. Acoustics Speech Signal Process 28:357-366.
23. Desai R, Liebenthal E, Waldron E, Binder JR. 2008. Left posterior temporal regions are sensitive to auditory categorization. J Cogn Neurosci. 20:1174-1188.
24. Dykstra AR, Chan AM, Quinn BT, Zepeda R, Keller CJ, Cormier J, Madsen JR, Eskandar EN, Cash SS. 2012. Individualized localization and cortical surface-based registration of intracranial electrodes. NeuroImage. 59:3563-3570.
25. Eliades SJ, Wang X. 2005. Dynamics of auditory-vocal interaction in monkey auditory cortex. Cereb Cortex. 15:1510-1523.
26. Fiebach CJ, Friederici AD, Muller K, von Cramon DY 2002. fMRI evidence for dual routes to the mental lexicon in visual word recognition. J Cogn Neurosci. 14:11-23.
27. Flinker A, Chang EF, Kirsch HE, Barbaro NM, Crone NE, Knight RT. 2010. Single-trial speech suppression of auditory cortex activity in humans. J Neurosci. 30:16643-16650.
28. Frost R. 1998. Toward a strong phonological theory of visual word recognition: true issues and false trails. Psychol Bull. 123:71-99.
29. Ganong WF III. 1980. Phonetic categorization in auditory word perception. J Exp Psychol Hum Percept Perform. 6:110-125.
30. Geschwind N, Levitsky W. 1968. Human brain: left-right asymmetries in temporal speech region. Science. 161:186-187.
31. Greenlee JD, Jackson AW, Chen F, Larson CR, Oya H, Kawasaki H, Chen H, Howard MA III. 2011. Human auditory cortical activation during self-vocalization. PLoS ONE. 6:e14744.
32. Hackett TA 2011. Information flow in the auditory cortical network. Hear Res. 271:133-146.
33. Halgren E, Dhond RP, Christensen N, Van Petten C, Marinkovic K, Lewine JD, Dale AM. 2002. N400-like magnetoencephalography responses modulated by semantic context, word frequency, and lexical class in sentences. NeuroImage. 17:1101-1116.
34. Halgren E, Wang C, Schomer DL, Knake S, Marinkovic K, Wu J, Ulbert I. 2006. Processing stages underlying word recognition in the anteroventral temporal lobe. NeuroImage. 30:1401-1413.
35. Heinks-Maldonado TH, Mathalon DH, Gray M, Ford JM. 2005. Finetuning of auditory cortex during speech production. Psychophy-siology. 42:180-190.
36. Heinks-Maldonado TH, Nagarajan SS, Houde JF. 2006. Magnetoencephalographic evidence for a precise forward model in speech production. Neuroreport. 17:1375-1379.
37. Heit G, Smith ME, Halgren E. 1988. Neural encoding of individual words and faces by the human hippocampus and amygdala. Nature. 333:773-775.
38. Hickok G, Poeppel D. 2007. The cortical organization of speech processing. Nat Rev. 8:393-402.
39. Hirano S, Naito Y, Okazawa H, Kojima H, Honjo I, Ishizu K, Yenokura Y, Nagahama Y, Fukuyama H, Konishi J. 1997. Cortical activation by monaural speech sound stimulation demonstrated by positron emission tomography. Exp Brain Res. 113:75-80.
40. Houde JF, Nagarajan SS, Sekihara K, Merzenich MM. 2002. Modulation of the auditory cortex during speech: an MEG study. J Cogn Neurosci. 14:1125-1138.
41. Howard D, Patterson K, Wise R, Brown WD, Friston K, Weiller C, Frackowiak R. 1992. The cortical localization of the lexicons. Positron emission tomography evidence. Brain. 115(Pt. 6):1769-1782.
42. Howard MA III, Volkov IO, Abbas PJ, Damasio H, Ollendieck MC, Granner MA. 1996. A chronic microelectrode investigation of the tonotopic organization of human auditory cortex. Brain Res. 724:260-264.
43. Kutas M, Federmeier KD. 2011. Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). Ann Rev Psychol. 62:621-647.
44. Lennie P. 2003. The cost of cortical computation. Curr Biol. 13:493-497.
45. Lund K, Burgess C. 1996. Producing high-dimensional semantic spaces from lexical co-occurrence. Behav Res Methods. 28:203-208.
46. Marinkovic K. 2004. Spatiotemporal dynamics of word processing in the human cortex. Neuroscientist. 10:142-152.
47. Marinkovic K, Dhond RP, Dale AM, Glessner M, Carr V, Halgren E. 2003. Spatiotemporal dynamics of modality-specific and supramodal word processing. Neuron. 38:487-497.
48. Maris E, Oostenveld R. 2007. Nonparametric statistical testing of EEGand MEG-data. J Neurosci Methods. 164:177-190.
49. Marslen-Wilson WD. 1987. Functional parallelism in spoken word-recognition. Cognition. 25:71-102.
50. McClelland JL, Elman JL. 1986. The TRACE model of speech perception. Cogn Psychol. 18:1-86.
51. Morton J. 1969. Interaction of information in word recognition. Psychol Rev. 76:165-178.
52. Newman RL, Connolly JF. 2004. Determining the role of phonology in silent reading using event-related brain potentials. Brain Res. 21:94-105.
53. Niznikiewicz M, Squires NK. 1996. Phonological processing and the role of strategy in silent reading: behavioral and electrophysiological evidence. Brain Lang. 52:342-364.
54. Norris D, McQueen JM, Cutler A. 2000. Merging information in speech recognition: feedback is never necessary. Behav Brain Sci. 23:299-325; discussion 325-370
55. Numminen J, Salmelin R, Hari R. 1999. Subject's own speech reduces reactivity of the human auditory cortex. Neurosci Lett. 265:119-122.
56. Obleser J, Boecker H, Drzezga A, Haslinger B, Hennenlotter A, Roettinger M, Eulitz C, Rauschecker JP. 2006. Vowel sound extraction in anterior superior temporal cortex. Hum Brain Mapp. 27:562-571.
57. Obleser J, Leaver AM, Vanmeter J, Rauschecker JP. 2010. Segregation of vowels and consonants in human auditory cortex: evidence for distributed hierarchical organization. Front Psychol. 1:232.
58. Ojemann GA, Schoenfield-McNeill J. 1999. Activity of neurons in human temporal cortex during identification and memory for names and words. J Neurosci. 19:5674-5682.
59. Olshausen BA, Field DJ. 2004. Sparse coding of sensory inputs. Curr Opin Neurobiol. 14:481-487.
60. Pasley BN, David SV, Mesgarani N, Flinker A, Shamma SA, Crone NE, Knight RT, Chang EF. 2012. Reconstructing speech from human auditory cortex. PLoS Biol. 10:e1001251.
61. Paus T, Perry DW, Zatorre RJ, Worsley KJ, Evans AC. 1996. Modulation of cerebral blood flow in the human auditory cortex during speech: role of motor-to-sensory discharges. Eur J Neurosci. 8:2236-2246.
62. Perani D, Dehaene S, Grassi F, Cohen L, Cappa SF, Dupoux E, Fazio F, Mehler J. 1996. Brain processing of native and foreign languages. Neuroreport. 7:2439-2444.
63. Perrone-Bertolotti M, Kujala J, Vidal JR, Hamame CM, Ossandon T, Bertrand O, Minotti L, Kahane P, Jerbi K, Lachaux J-P. 2012. How silent is silent reading? Intracerebral evidence for top-down activation of temporal voice areas during reading. J Neurosci. 32:17554-17562.
64. Peyrache A, Dehghani N, Eskandar EN, Madsen JR, Anderson WS, Donoghue JA, Hochberg LR, Halgren E, Cash SS, Destexhe A. 2012. Spatiotemporal dynamics of neocortical excitation and inhibition during human sleep. Proc Natl Acad Sci USA. 109:1731-1736.
65. Price CJ, Wise RJ, Warburton EA, Moore CJ, Howard D, Patterson K, Frackowiak RS, Friston KJ. 1996. Hearing and saying. The functional neuro-anatomy of auditory word processing. Brain. 119(Pt. 3):919-931.
66. Rauschecker JP 1998. Cortical processing of complex sounds. Curr Opin Neurobiol. 8:516-521.
67. Rauschecker JP, Scott SK. 2009. Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci. 12:718-724.
68. Ravagnati L, Halgren E, Babb TL, Crandall PH. 1979. Activity of human hippocampal formation and amygdala neurons during sleep. Sleep. 2:161-173.
69. Saur D, Kreher BW, Schnell S, Kummerer D, Kellmeyer P, Vry MS, Umarova R, Musso M, Glauche V, Abel S et al. 2008. Ventral and dorsal pathways for language. Proc Natl Acad Sci USA. 105:18035-18040.
70. Scott SK, Blank CC, Rosen S, Wise RJ. 2000. Identification of a pathway for intelligible speech in the left temporal lobe. Brain. 123(Pt. 12):2400-2406.
71. Scott SK, Rosen S, Lang H, Wise RJ. 2006. Neural correlates of intelligibility in speech investigated with noise vocoded speech-a positron emission tomography study. J Acoust Soc Am. 120:1075-1083.
72. Seidenberg MS 1985. The time course of phonological code activation in two writing systems. Cognition. 19:1-30.
73. Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M. 1995. Speech recognition with primarily temporal cues. Science. 270:303-304.
74. Steinschneider M, Nourski KV, Kawasaki H, Oya H, Brugge JF, Howard MA III. 2011. Intracranial study of speech-elicited activity on the human posterolateral superior temporal gyrus. Cereb Cortex. 21:2332-2347.
75. Tanaka K. 1996. Inferotemporal cortex and object vision. Ann Rev Neurosci. 19:109-139.
76. Tankus A, Fried I, Shoham S. 2012. Structured neuronal encoding and decoding of human speech features. Nat Commun. 3:1015.
77. Theunissen FE, David SV, Singh NC, Hsu A, Vinje WE, Gallant JL. 2001. Estimating spatio-temporal receptive fields of auditory and visual neurons from their responses to natural stimuli. Network. 12:289-316.
78. Tourville JA, Reilly KJ, Guenther FH. 2008. Neural mechanisms underlying auditory feedback control of speech. NeuroImage. 39:1429-1443.
79. Travis KE, Leonard MK, Chan AM, Torres C, Sizemore ML, Qu Z, Eskandar E, Dale AM, Elman JL, Cash SS et al. 2012. Independence of early speech processing from word meaning. Cereb Cortex. doi:10.1093/cercor/bhs228.
80. Vinckier F, Dehaene S, Jobert A, Dubus JP, Sigman M, Cohen L. 2007. Hierarchical coding of letter strings in the ventral stream: dissecting the inner organization of the visual word-form system. Neuron. 55:143-156.
81. Warren JD, Scott SK, Price CJ, Griffiths TD. 2006. Human brain mechanisms for the early analysis of voices. NeuroImage. 31:1389-1397.
82. Warren RM 1970. Perceptual restoration of missing speech sounds. Science. 167:392-393.
83. Wernicke C. 1874. Der aphasische Symptomencomplex: eine psychologische Studie auf anatomischer Basis. Breslau: Cohn & Weigert.
84. Wessinger CM, VanMeter J, Tian B, Van Lare J, Pekar J, Rauschecker JP. 2001. Hierarchical organization of the human auditory cortex revealed by functional magnetic resonance imaging. J Cogn Neurosci. 13:1-7.
85. Yvert G, Perrone-Bertolotti M, Baciu M, David O. 2012. Dynamic causal modeling of spatiotemporal integration of phonological and semantic processes: an electroencephalographic study. J Neurosci. 32:4297-4306.
86. Zatorre RJ, Bouffard M, Belin P. 2004. Sensitivity to auditory object features in human temporal neocortex. J Neurosci. 24:3637-3642.
87. Ziegler JC, Benraiss A, Besson M. 1999. From print to meaning: an electrophysiological investigation of the role of phonology in accessing word meaning. Psychophysiology. 36:775-785.