Representation of speech categories in the primate auditory cortex

Journal of Neurophysiology

Volumn 105, Issue 6, 2011, Pages 2634-2646

  Tsunada, Joji ^a   Lee, Jung Hoon ^a   Cohen, Yale E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Categorization; Decision making; Phoneme; Rhesus monkey; Superior temporal gyrus

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BRAIN NERVE CELL; CONTROLLED STUDY; DECISION MAKING; MALE; NEUROANATOMY; NONHUMAN; PHONEME; PREFRONTAL CORTEX; PRIORITY JOURNAL; RHESUS MONKEY; SECONDARY AUDITORY CORTEX; SPEECH; SPIKE WAVE; SUPERIOR TEMPORAL GYRUS;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY CORTEX; AUDITORY PATHWAYS; AUDITORY PERCEPTION; BRAIN MAPPING; CHOICE BEHAVIOR; MACACA MULATTA; MALE; NEURONS; PHONETICS; PSYCHOACOUSTICS; PSYCHOMETRICS; REACTION TIME; REGRESSION ANALYSIS; ROC CURVE;

EID: 79959346369     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00037.2011     Document Type: Article

References (90)

1. Ashby FG, Spiering BJ. The neurobiology of category learning. Behav Cogn Neurosci Rev 3: 101-113, 2004.
2. Barlow HB, Levick WR, Yoon M. Responses of single quanta of light in retinal ganglion cells of the cat. Vision Res, Suppl 3: 87-101, 1971.
3. Binder JR, Liebenthal E, Possing ET, Medler DA, Ward BD. Neural correlates of sensory and decision processes in auditory object identification. Nat Neurosci 7: 295-301, 2004.
4. Britten KH, Newsome WT, Shadlen MN, Celebrini S, Movshon JA. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis Neurosci 13: 87-100, 1996.
5. Britten KH, Shadlen MN, Newsome WT, Movshon JA. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci 12: 4745-4765, 1992.
6. Burton MW, Small SL. Functional neuroanatomy of segmenting speech and nonspeech. Cortex 42: 644-665, 2006.
7. Celebrini S, Newsome WT. Microstimulation of extrastriate area MST influences performance on a direction discrimination task. J Neurophysiol 73: 437-448, 1995.
8. Celebrini S, Newsome WT. Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey. J Neurosci 14: 4109-4124, 1994.
9. Celsis P, Doyon B, Boulanouar K, Pastor J, Démonet JF, Nespoulous JL. ERP correlates of phoneme perception in speech and sound contexts. Neuroreport 14: 1523-1527, 1999.
10. Chang EF, Rieger JW, Johnson K, Berger MS, Barbaro NM, Knight RT. Categorical speech representation in human superior temporal gyrus. Nat Neurosci 13: 1428-1432, 2010.
11. Cohen YE, Russ BE, Davis SJ, Baker AE, Ackelson AL, Nitecki R. A functional role for the ventrolateral prefrontal cortex in non-spatial auditory cognition. Proc Natl Acad Sci USA 106: 20045-20050, 2009.
12. Cohen YE, Theunissen F, Russ BE, Gill P. Acoustic features of rhesus vocalizations and their representation in the ventrolateral prefrontal cortex. J Neurophysiol 97: 1470-1484, 2007.
13. Cohn TE, Green DG, Tanner WP. Receiver operating characteristic analysis: Application to the study of quantum fluctuation in optic nerve of Rana pipiens. J Gen Physiol 66: 583-616, 1971.
14. Engineer CT, Perez CA, Chen YH, Carraway RS, Reed AC, Shetake JA, Jakkamsetti V, Chang KQ, Kilgard MP. Cortical activity patterns predict speech discrimination ability. Nat Neurosci 11: 603-608, 2008.
15. Ferrera VP, Yanike M, Cassanello C. Frontal eye field neurons signal changes in decision criteria. Nat Neurosci 12: 1458-1462, 2009.
16. Freedman DJ, Assad JA. Experience-dependent representation of visual categories in parietal cortex. Nature 443: 85-88, 2006.
17. Freedman DJ, Riesenhuber M, Poggio T, Miller EK. Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291: 312-316, 2001.
18. Freedman DJ, Riesenhuber M, Poggio T, Miller EK. A comparison of primate prefrontal and inferior temporal cortices during visual categorization. J Neurosci 23: 5235-5246, 2003.
19. Freedman DJ, Riesenhuber M, Poggio T, Miller EK. Visual categorization and the primate prefrontal cortex: neurophysiology and behavior. J Neurophysiol 88: 929-941, 2002.
20. Ghazanfar AA, Maier JX, Hoffman KL, Logothetis NK. Multisensory integration of dynamic faces and voices in rhesus monkey auditory cortex. J Neurosci 25: 5004-5012, 2005.
21. Gifford GW III, MacLean KA, Hauser MD, Cohen YE. The neurophysiologyof functionally meaningful categories: macaque ventrolateral prefrontal cortex plays a critical role in spontaneous categorization of speciesspecific vocalizations. J Cogn Neurosci 17: 1471-1482, 2005.
22. Gold JI, Shadlen MN. The neural basis of decision making. Ann Rev Neurosci 30: 535-574, 2007.
23. Green DM, Swets JA. Signal Detection Theory and Psychophysics. New York: John Wiley and Sons, 1966.
24. Griffiths TD, Warren JD. What is an auditory object? Nat Rev Neurosci 5: 887-892, 2004.
25. Grunewald A, Bradley DC, Andersen RA. Neural correlates of structurefrom- motion perception in macaque V1 and MT. J Neurosci 22: 6195-6207, 2002.
26. Gu Y, DeAngelis GC, Angelaki DE. A functional link between area MSTd and heading perception based on vestibular signals. Nat Neurosci 10: 1038-1047, 2007.
27. Guenther FH, Nieto-Castanon A, Ghosh SS, Tourville JA. Representation of sound categories in auditory cortical maps. J Speech Lang Hear Res 47: 46-57, 2004.
28. Hackett TA, Stepniewska I, Kaas JH. Prefrontal connections of the parabelt auditory cortex in macaque monkeys. Brain Res 817: 45-58, 1999.
29. Hernández A, Nácher V, Luna R, Zainos A, Lemus L, Alvarez M, Vázquez Y, Camarillo L, Romo R. Decoding a perceptual decision process across cortex. Neuron 29: 300-314, 2010.
30. Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci 8: 393-402, 2007.
31. Horwitz GD, Newsome WT. Separate signals for target selection and movement specification in the superior colliculus. Science 284: 1158-1161, 1999.
32. Husain FT, Fromin SJ, Pursley RH, Hosey LA, Braun A, Horwitz B. Neural bases of categorization of simple speech and nonspeech sounds. Hum Brain Mapp 27: 636-651, 2006.
33. Judge SJ, Richmond BJ, Chu FC. Implantation of magnetic search coils for measurement of eye position: an improved method. Vis Res 20: 535-538, 1980.
34. Kaas JH, Hackett TA. "What" and "where" processing in auditory cortex. Nat Neurosci 2: 1045-1047, 1999.
35. Kawahara H, Masuda-Katsuse I, de Cheveigne A. Restructuring speech representations using a pitch-adaptive time-frequency smoothing and an instantaneous-frequency-based F0 extraction. Speech Comm 27: 187-199, 1999.
36. Kayser J, Tenke CE, Bruder GE. Dissociation of brain ERP topographies for tonal and phonetic oddball tasks. Psychophysiology 35: 576-590, 1998.
37. Kikuchi Y, Horwitz B, Mishkin M. Hierarchical auditory processing directed rostrally along the monkey's supratemporal plane. J Neurosci 30: 13021- 13030, 2010.
38. Kim JN, Shadlen MN. Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat Neurosci 2: 176-185, 1999.
39. Kluender KR, Alexander JM. Perception of speech sounds. In: The Senses: A Comprehensive Reference, edited by Basbaum AI, Kaneko A, Shepherd GM, Westheimer G, Albright TD, Masland RH, Dallos P, Oertel D, Firestein S, Beauchamp GK, Bushnell MC, Kaas JH, Gardener E. San Diego, CA: Elsevier, 2008, p. 829-176-860.
40. Kluender KR, Diehl RL, Killeen P. Japanese quail can learn phonetic categories. Science 237: 1195-1197, 1987.
41. Koida K, Komatsu H. Effects of task demands on the responses of colorselective neurons in the inferior temporal cortex. Nat Neurosci 10: 108-116, 2007.
42. Kuhl PK, Miller JD. Speech perception by the chinchilla: voiced-voiceless distinction in alveolar plosive consonants. Science 190: 69-72, 1975.
43. Kuhl PK, Padden DM. Enhanced discriminability at the phonetic boundaries for the place feature in macaques. J Acoust Soc Am 73: 1003-1010, 1983.
44. Kuhl PK, Padden DM. Enhanced discriminability at the phonetic boundaries for the voicing feature in macaques. Percept Psychophys 32: 542-550, 1982.
45. Leaver AM, Rauschecker JP. Cortical representation of natural complex sounds: effects of acoustic features and auditory object category. J Neurosci 30: 7604-7612, 2010.
46. Lee JH, Russ BE, Orr LE, Cohen YE. Prefrontal activity predicts monkeys' decisions during an auditory category task. Fron Integr Neurosci 3: 2009.
47. Lemus L, Hernandez A, Romo R. Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex. Proc Natl Acad Sci USA 106: 9471-9476, 2009a.
48. Lemus L, Hernández A, Romo R. Neural encoding of auditory discrimination in ventral premotor cortex. Proc Natl Acad Sci USA 106: 14650-14655, 2009b.
49. Liberman AM, Harris KS, Hoffman HS, Griffith BC. The discrimination of speech sounds within and across phoneme boundaries. J Exp Psychol 54: 358-368, 1957.
50. Liebenthal E, Desai R, Ellingson MM, Ramachandran B, Desai A, Binder JR. Specialization along the left superior temporal sulcus for auditory categorization. Cereb Cortex 2-: 2958-2970, 2010.
51. Locasto PC, Krebs-Noble D, Gullapalli RP, Burton MW. An fMRI investigation of speech and tone segmentation. J Cogn Neurosci 16: 1612-1624, 2004.
52. Mesgarani N, David SV, Fritz JB, Shamma SA. Phoneme representation and classification in primary auditory cortex. J Acoust Soc Am 123: 899-909, 2008.
53. Miller CT, Cohen YE. Vocalization processing. In: Primate Neuroethology, edited by Ghazanfar A, Platt ML. Oxford, UK: Oxford University Press, 2010.
54. Newsome WT, Pare EB. A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci 8: 2201-2211, 1988.
55. Novak GP, Ritter W, Vaughan HG Jr, Wiznitzer ML. Differentiation of negative event-related potentials in an auditory discrimination task. Electroencephalogr Clin Neurophysiol 75: 255-275, 1990.
56. Obleser J, Leaver AM, Van Meter J, Rauschecker JP. Segregation of vowels and consonants in human auditory cortex: evidence for distributed hierarchical organization. Front Psychol Aud Cog Neurosci 1: 1-14, 2010.
57. Obleser J, Zimmermann J, Van Meter J, Rauschecker JP. Multiple stages of auditory speech perception reflected in event-related FMRI. Cereb Cortex 17: 2251-2257, 2007.
58. Parker AJ, Newsome WT. Sense and the single neuron: probing the physiology of perception. Ann Rev Neurosci 21: 227-277, 1998.
59. Poeppel D, Guillemin A, Thompson J, Fritz J, Bavelier D, Braun AR. Auditory lexical decision, categorical perception, and FM direction discrimination differentially engage left and right auditory cortex. Neuropsychologia 42: 183-200, 2004.
60. Purushothaman G, Bradley DC. Neural population code for fine perceptual decisions in area MT. Nat Neurosci 8: 99-106, 2005.
61. Quiroga RQ, Nadasy Z, Ben-Shaul M. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16: 1661-1687, 2004.
62. Raizada RD, Poldrack RA. Selective amplification of stimulus differences during categorical processing of speech. Neuron 56: 726-740, 2007.
63. Rauschecker JP. Parallel processing in the auditory cortex of primates. Audiol Neurootol 3: 86-103, 1998.
64. Rauschecker JP, Scott SK. Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 12: 718- 724, 2009.
65. Rauschecker JP, Tian B. Mechanisms and streams for processing of "what" and "where" in auditory cortex. Proc Natl Acad Sci USA 97: 11800-11806, 2000.
66. Recanzone GH, Cohen YE. Serial and parallel processing in the primate auditory cortex revisited. Behav Brain Res 5: 1-6, 2010.
67. Roitman JD, Shadlen MN. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J Neurosci 22: 9475-9489, 2002.
68. Romanski LM, Averbeck BB. The primate cortical auditory system and neural representation of conspecific vocalizations. Ann Rev Neurosci 2009.
69. Romanski LM, Bates JF, Goldman-Rakic P.S Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 403: 141-157, 1999a.
70. Romanski LM, Tian B, Fritz J, Mishkin M, Goldman-Rakic PS, Rauschecker JP. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci 2: 1131-1136, 1999b.
71. Romo R, Hernández A, Zainos A. Neuronal correlates of a perceptual decision in ventral premotor cortex. Neuron 8: 165-173, 2004.
72. Russ BE, Ackelson AL, Baker AE, Cohen YE. Coding of auditory-stimulus identity in the auditory non-spatial processing stream. J Neurophysiol 99: 87-95, 2008a.
73. Russ BE, Orr LE, Cohen YE. Auditory category learning in rhesus macaques. In: Program No 3445 2006 Neuroscience Meeting Planner. Atlanta, GA: Society for Neuroscience, 2006.
74. Russ BE, Orr LE, Cohen YE. Prefrontal neurons predict choices during an auditory same-different task. Curr Biol 18: 1483-1488, 2008b.
75. Salzman CD, Britten KH, Newsome WT. Cortical microstimulation influences perceptual judgements of motion direction [published erratum appears in Nature 1990 Aug 9;346(6284):589] [see comments]. Nature 346: 174- 177, 1990.
76. Salzman CD, Murasugi CM, Britten KH, Newsome WT. Microstimulation in visual area MT: effects on direction discrimination performance. J Neurosci 12: 2331-2355, 1992.
77. Selezneva E, Scheich H, Brosch M. Dual time scales for categorical decision making in auditory cortex. Curr Biol 16: 2428-2433, 2006.
78. Shadlen MN, Britten KH, Newsome WT, Movshon JA. A computational analysis of the relationship between neuronal and behavioral responses to visual motion. J Neurosci 16: 1486-1510, 1996.
79. Shadlen MN, Newsome WT. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J Neurophysiol 86: 1916-1936, 2001.
80. Sinnott JM, Gilmore CS. Perception of place-of-articulation information in natural speech by monkeys vs. humans. Percept Psychophys 66: 1341-1350, 2004.
81. Steinschneider M, Fishman YI. Enhanced physiologic discriminability of stop consonants with prolonged formant transitions in awake monkeys based on the tonotopic organization of primary auditory cortex. Hear Res 27: 103-114, 2010.
82. Steinschneider M, Fishman YI, Arezzo JC. Representation of the voice onset time (VOT) speech parameter in population responses within primary auditory cortex of the awake monkey. J Acoust Soc Am 114: 307-321, 2003.
83. Steinschneider M, Schroeder CE, Arezzo JC, Vaughan HG Jr. Physiologic correlates of the voice onset time boundary in primary auditory cortex (A1) of the awake monkey: temporal response patterns. Brain Lang 48: 326-340, 1995.
84. 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.
85. Steinschneider M, Volkov IO, Fishman YI, Oya H, Arezzo JC, Howard MA, 3rd. Intracortical responses in human and monkey primary auditory cortex support a temporal processing mechanism for encoding of the voice onset time phonetic parameter. Cereb Cortex 15: 170-186, 2005.
86. Steinschneider M, Volkov IO, Noh MD, Garell PC, Howard MA, 3rd. Temporal encoding of the voice onset time phonetic parameter by field potentials recorded directly from human auditory cortex. J Neurophysiol 82: 2346-2357, 1999.
87. Tolhurst DJ, Movshon JA, Dean AF. The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res 23: 775-785, 1983.
88. Wolmetz M, Poeppel D, Rapp B. What does the right hemisphere know about phoneme categories? J Cogn Neurosci 23: 1-18, 2010.
89. Woods DL, Alho K, Algazi A. Stages of auditory feature conjunction: an event-related brain potential study. J Exp Psychol Hum Percept Perform 20: 81-94, 1994.
90. Zatorre RR, Binder editors JR. The Human Auditory System. San Diego, CA: Academic, 2000, p. 36581-402.