Coding of repetitive transients by auditory cortex on posterolateral superior temporal gyrus in humans: An intracranial electrophysiology study

Journal of Neurophysiology

Volumn 109, Issue 5, 2013, Pages 1283-1295

  Nourski, Kirill V ^a   Brugge, John F ^a,b   Reale, Richard A ^a,b   Kovach, Christopher K ^a   Oya, Hiroyuki ^a   Kawasaki, Hiroto ^a   Jenison, Rick L ^b   Howard, Matthew A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Averaged evoked potential; Click train; Electrocorticography; High gamma; Phase locking

Indexed keywords

ADULT; ARTICLE; AUDITORY CORTEX; AUDITORY RESPONSE; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; CLINICAL ARTICLE; EPILEPSY; EVOKED AUDITORY RESPONSE; FEMALE; GAMMA RHYTHM; HUMAN; MALE; NEUROSURGERY; PATIENT MONITORING; PRIORITY JOURNAL; SUPERIOR TEMPORAL GYRUS; WAVEFORM;

ACOUSTIC STIMULATION; ADULT; AUDITORY CORTEX; BRAIN WAVES; EPILEPSY; EVOKED POTENTIALS, AUDITORY; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MALE; MIDDLE AGED; TEMPORAL LOBE;

EID: 84874596110     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00718.2012     Document Type: Article

References (83)

1. Bao S, Chang EF, Woods J, Merzenich MM. Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nat Neurosci 7: 974-981, 2004.
2. Benjamini Y, Drai D, Elmer G, Kafkari N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279-284, 2001.
3. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc B Methodol 57: 289-300, 1995.
4. Brugge JF, Nourski KV, Oya H, Reale RA, Kawasaki H, Steinschneider M, Howard MA III. Coding of repetitive transients by auditory cortex of Heschl's gyrus of human. J Neurophysiol 102: 2358-2374, 2009.
5. Brugge JF, Volkov IO, Garell PC, Reale RA, Howard MA III. Functional connections between auditory cortex on Heschl's gyrus and on the lateral superior temporal gyrus in humans. J Neurophysiol 90: 3750-3763, 2003.
6. Brugge JF, Volkov IO, Oya H, Kawasaki H, Reale RA, Fenoy A, Steinschneider M, Howard MA III. Functional localization of auditory cortical fields of human: click-train stimulation. Hear Res 238: 12-24, 2008.
7. Brugge JF, Volkov IO, Reale RA, Garell PC, Kawasaki H, Oya H, Li Q, Howard MA III. The posterolateral superior temporal auditory field in humans: functional organization and connectivity. In: Auditory Cortex. A Synthesis of Human and Animal Research, edited by Konig R, Heil P, Budinger E, and Scheich H. Mahwah, NJ: Erlbaum, 2005, p. 145-162.
8. Buszaki G. Rhythms of the Brain. New York: Oxford University Press, 2006.
9. Chavez M, Besserve M, Adam C, Martinerie J. Towards a proper estimation of phase synchronization from time series. J Neurosci Methods 154: 149-160, 2006.
10. Chevillet M, Riesenhuber M, Rauschecker JP. Functional correlates of the anterolateral processing hierarchy in human auditory cortex. J Neurosci 31: 9345-9352, 2011.
11. Chiry O, Tardif E, Magistretti PJ, Clarke S. Patterns of calcium-binding proteins support parallel and hierarchical organization of human auditory areas. Eur J Neurosci 17: 397-410, 2003.
12. Crone NE, Boatman D, Gordon B, Hao L. Induced electrocorticographic gamma activity during auditory perception. Clin Neurophysiol 112: 565-582, 2001.
13. de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA. Thalamic connections of auditory cortex in marmoset monkeys: lateral belt and parabelt regions. Anat Rec (Hoboken) 295: 822-836, 2012.
14. Doesburg SM, Emberson LL, Rahi A, Cameron D, Ward LM. Asynchrony from synchrony: long-range gamma-band neural synchrony accompanies perception of audiovisual speech asynchrony. Exp Brain Res 185: 11-20, 2008.
15. Edwards E, Soltani M, Kim W, Dalal SS, Nagarajan SS, Berger MS, Knight RT. Comparison of time-frequency responses and the event-related potential to auditory speech stimuli in human cortex. J Neurophysiol 102: 377-386, 2009.
16. Frien A, Eckhorn R, Bauer R, Woelbern T, Gabriel A. Fast oscillations display sharper orientation tuning than slower components of the same recordings in striate cortex of the awake monkey. Eur J Neurosci 12: 1453-1465, 2000.
17. Fullerton BC, Pandya DN. Architectonic analysis of the auditory-related areas of the superior temporal region in human brain. J Comp Neurol 504: 470-498, 2007.
18. Giraud AL, Lorenzi C, Ashburner J, Wable J, Johnsrude I, Frackowiak R, Kleinschmidt A. Representation of the temporal envelope of sounds in the human brain. J Neurophysiol 84: 1588-1598, 2000.
19. Gourévitch B, Le Bouquin-Jeannès R, Faucon G, Liégeois-Chauvel C. Temporal envelope processing in the human auditory cortex: response and interconnections of auditory cortical areas. Hear Res 237: 1-18, 2008.
20. Hackett TA. Anatomical organization of the auditory cortex. J Am Acad Audiol 19: 774-779, 2008.
21. Hackett TA. Information flow in the auditory cortical network. Hear Res 271: 133-146, 2011.
22. Hackett TA. Organization and correspondence of the auditory cortex of humans and nonhuman primates. In: Evolution of the Nervous System, edited by Kaas JH. Oxford, UK: Elsevier, 2007, p. 109-119.
23. Hackett TA. The comparative anatomy of the primate auditory cortex. In: Primate Audition: Ethology and Neurobiology, edited by Ghazanfar AA. Boca Raton, FL: CRC, 2003, p. 199-219.
24. Hackett TA, Preuss TM, Kaas JH. Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. J Comp Neurol 441: 197-222, 2001.
25. Harms MP, Melcher JR. Sound repetition rate in the human auditory pathway: representations in the waveshape and amplitude of fMRI activation. J Neurophysiol 88: 1433-1450, 2002.
26. Heil P. Coding of temporal onset envelope in the auditory system. Speech Commun 41: 123-134, 2003.
27. Heil P, Irvine DR. First-spike timing of auditory-nerve fibers and comparison with auditory cortex. J Neurophysiol 78: 2458-2454, 1997.
28. Hipp JF, Engel AK, Siegel M. Oscillatory synchronization in large-scale cortical networks predicts perception. Neuron 69: 387-396, 2011.
29. Howard MA, Nourski KV, Brugge JF. Invasive research methods. In: Human Auditory Cortex, edited by Poeppel D, Overath T, Popper AN, and Fay RR. New York: Springer Science + Business Media, 2012, p. 39-67.
30. Howard MA, Volkov IO, Abbas PJ, Damasio H, Ollendieck MC, Granner MA. A chronic microelectrode investigation of the tonotopic organization of human auditory cortex. Brain Res 724: 260-264, 1996.
31. Howard MA, Volkov IO, Mirsky R, Garell PC, Noh MD, Granner M, Damasio H, Steinschneider M, Reale RA, Hind JE, Brugge JF. Auditory cortex on the posterior superior temporal gyrus of human cerebral cortex. J Comp Neurol 416: 76-92, 2000.
32. Hutsler JJ, Gazzaniga MS. Acetylcholinesterase staining in human auditory and language cortices: regional variation of structural features. Cereb Cortex 6: 260-270, 1996.
33. Imaizumi K, Priebe NJ, Sharpee TO, Cheung SW, Schreiner CE. Encoding of temporal information by timing, rate, and place in cat auditory cortex. PLoS One 5: e11531, 2010.
34. Jenkinson M, Bannister P, Brady J, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17: 825-841, 2002.
35. Jervis BW, Nichols MJ, Johnson TE, Allen E, Hudson NR. A fundamental investigation of the composition of auditory evoked potentials. IEEE Trans Biomed Eng 30: 43-50, 1983.
36. Joris PX, Schreiner CE, Rees A. Neural processing of amplitude-modulated sounds. Physiol Rev 84: 541-577, 2004.
37. Kaas JH, Hackett TA. Subdivisions and connections of auditory cortex in primates: a working model. In: Auditory Cortex. A Synthesis of Human and Animal Research, edited by Konig R, Heil P, Budinger E, and Scheich H. Mahwah, NJ: Erlbaum, 2005, p. 7-26.
38. Krumbholz K, Patterson RD, Pressnitzer D. The lower limit of pitch as determined by rate discrimination. J Acoust Soc Am 108: 1170-1180, 2000.
39. Kuwada S, Batra R, Maher VL. Scalp potentials of normal and hearingimpaired subjects in response to sinusoidally amplitude-modulated tones. Hear Res 21: 179-192, 1986.
40. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ. Measuring phase synchrony in brain signals. Hum Brain Mapp 8: 194-208, 1999.
41. Langner G. Periodicity coding in the auditory system. Hear Res 60: 115-142, 1992.
42. Law SK, Nunez PL, Wijesinghe RS. High-resolution EEG using spline generated surface Laplacians on spherical and ellipsoidal surfaces. IEEE Trans Biomed Eng 40: 145-153, 1993.
43. Liang L, Lu T, Wang X. Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates. J Neurophysiol 87: 2237-2261, 2002.
44. Liégeois-Chauvel C, Lorenzi C, Trébuchon A, Régis J, Chauvel P. Temporal envelope processing in the left and right auditory cortices. Cereb Cortex 14: 731-740, 2004.
45. Liegeois-Chauvel C, Musolino A, Chauvel P. Localization of the primary auditory area in man. Brain 114: 139-151, 1991.
46. Liu J, Newsome WT. Local field potential in cortical area MT: stimulus tuning and behavioral correlations. J Neurosci 26: 7779-7790, 2006.
47. Lu T, Liang L, Wang X. Temporal and rate representations of time-varying signals in the auditory cortex of awake primates. Nat Neurosci 4: 1131-1138, 2001.
48. Mardia KV, Jupp PE. Directional Statistics. Hoboken, NJ: John Wiley & Sons, 2000.
49. Mukamel R, Fried I. Human intracranial recordings and cognitive neuroscience. Annu Rev Psychol 63: 511-537, 2012.
50. Nakahara H, Yamada S, Mizutani T, Murayama S. Identification of the primary auditory field in archival human brain tissue via immunocytochemistry of parvalbumin. Neurosci Lett 286: 29-32, 2000.
51. Nir Y, Fisch L, Mukamel R, Gelbard-Sagiv H, Arieli A, Fried I, Malach R. Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr Biol 17: 1275-1285, 2007.
52. Nourski K, Brugge J, Reale R, Kawasaki H, Oya H, Kovach C, Howard M. Responses to repetitive transients within human lateral superior temporal gyrus: an intracranial electrophysiology study. Association for Research in Otolaryngology 2011 MidWinter Meeting, February 19-23, 2011, Baltimore, MD. Assoc Res Otolaryngol Abstr, 2011.
53. Nourski KV, Brugge JF. Representation of temporal sound features in the human auditory cortex. Rev Neurosci 22: 187-203, 2011.
54. Nunez P. Electric Fields of the Brain. New York: Oxford University Press, 1981.
55. Nunez PL, Pilgreen KL. The Spline-Laplacian in clinical neurophysiology: a method to improve EEG spatial resolution. J Clin Neurophysiol 8: 397-413, 1991.
56. Oya H, Kawasaki H, Howard MA III, Adolphs R. Electrophysiological responses in the human amygdala discriminate emotion categories of complex visual stimuli. J Neurosci 22: 9502-9512, 2002.
57. Pawitan Y. In All Likelihood: Statistical Modeling and Inference Using Likelihood. Oxford, UK: Clarendon, 2001.
58. Perrin F, Pernier J, Bertrand O, Giard MH, Echallier JF. Mapping of scalp potentials by surface spline interpolation. Electroencephalogr Clin Neurophysiol 66: 75-81, 1987.
59. Phillips DP. Sensory representations, the auditory cortex, and speech perception. Semin Hear 19: 319-331, 1998.
60. Phillips DP, Farmer ME. Acquired word deafness, and the temporal grain of sound representation in the primary auditory cortex. Behav Brain Res 40: 85-94, 1990.
61. Phillips DP, Hall SE. Response timing constraints on the cortical representation of sound time structure. J Acoust Soc Am 88: 1403-1411, 1990.
62. Rauschecker JP, Scott SK. Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 12: 718-724, 2009.
63. Reale RA, Calvert GA, Thesen T, Jenison RL, Kawasaki H, Oya H, Howard MA, Brugge JF. Auditory-visual processing represented in the human superior temporal gyrus. Neuroscience 145: 162-184, 2007.
64. Reddy CG, Dahdaleh NS, Albert G, Chen F, Hansen D, Nourski K, Kawasaki H, Oya H, Howard MA III. A method for placing Heschl gyrus depth electrodes. J Neurosurg 112: 1301-1307, 2010.
65. Rees A, Green GG, Kay RH. Steady-state evoked responses to sinusoidally amplitude-modulated sounds recorded in man. Hear Res 23: 123-133, 1986.
66. Rivier F, Clarke S. Cytochrome oxidase, acetylcholinesterase, and NADPHdiaphorase staining in human supratemporal and insular cortex: evidence for multiple auditory areas. Neuroimage 6: 288-304, 1997.
67. Ross B, Borgmann C, Draganova R, Roberts LE, Pantev C. A highprecision magnetoencephalographic study of human auditory steady-state responses to amplitude-modulated tones. J Acoust Soc Am 108: 679-681, 2000.
68. Schnupp JW, Hall TM, Kokelaar RF, Ahmed B. Plasticity of temporal pattern codes for vocalization stimuli in primary auditory cortex. J Neurosci 26: 4785-4795, 2006.
69. Senkowski D, Talsma D, Herrmann CS, Woldorff MG. Multisensory processing and oscillatory gamma responses: effects of spatial selective attention. Exp Brain Res 166: 411-426, 2005.
70. Steinschneider M, Nourski KV, Kawasaki H, Oya H, Brugge JF, Howard MA III. Intracranial study of speech-elicited activity on the human posterolateral superior temporal gyrus. Cereb Cortex 21: 2332-2347, 2011.
71. Steinschneider M, Reser DH, Fishman YI, Schroeder CE, Arezzo JC. Click train encoding in primary auditory cortex of the awake monkey: evidence for two mechanisms subserving pitch perception. J Acoust Soc Am 104: 2935-2955, 1998.
72. Steinschneider M, Schroeder CE, Arezzo JC, Vaughan HG Jr. Speechevoked activity in primary auditory cortex: effects of voice onset time. Electroencephalogr Clin Neurophysiol 92: 30-43, 1994.
73. Steinschneider M, Tenke CE, Schroeder CE, Javitt DC, Simpson GV, Arezzo JC, Vaughan HG Jr. Cellular generators of the cortical auditory evoked potential initial component. Electroencephalogr Clin Neurophysiol 84: 196-200, 1992.
74. Sweet RA, Dorph-Petersen KA, Lewis DA. Mapping auditory core, lateral belt, and parabelt cortices in the human superior temporal gyrus. J Comp Neurol 491: 270-289, 2005.
75. Tan AY, Zhang LI, Merzenich MM, Schreiner CE. Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol 92: 630-643, 2004.
76. Vaughan HG Jr. The relationship of brain activity to scalp recordings of event-related potentials. In: Average Evoked Potentials. Methods, Results and Evaluations, edited by Donchin E and Lindsley DB. Washington, DC: National Aeronautics and Space Administration, 1969, p. 45-75.
77. Vaughan HG Jr, Arezzo JC. The neural basis of event-related potentials. In: Human Event-Related Potentials, edited by Picton TW. Amsterdam: Elsevier, 1988, vol. 3, p. 45-96.
78. Wallace MN, Johnston PW, Palmer AR. Histochemical identification of cortical areas in the auditory region of the human brain. Exp Brain Res 143: 499-508, 2002.
79. Wang X. Neural coding strategies in auditory cortex. Hear Res 229: 81-93, 2007.
80. Wang X, Lu T, Bendor D, Bartlett E. Neural coding of temporal information in auditory thalamus and cortex. Neuroscience 157: 484-494, 2008.
81. Wang X, Lu T, Liang L. Cortical processing of temporal modulations. Speech Commun 41: 107-121, 2003.
82. Wehr M, Zador AM. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426: 442-446, 2003.
83. Whittingstall K, Logothetis NK. Frequency-band coupling in surface EEG reflects spiking activity in monkey visual cortex. Neuron 64: 281-289, 2009.