Human superior temporal gyrus organization of spectrotemporal modulation tuning derived from speech stimuli

Journal of Neuroscience

Volumn 36, Issue 6, 2016, Pages 2014-2026

  Hullett, Patrick W ^a,b   Hamilton, Liberty S ^b,c   Mesgarani, Nima ^b,c   Schreiner, Christoph E ^a,b   Chang, Edward F ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Functional organization; Human STG; Human superior temporal gyrus; Modulation tuning; Modulotopic; Spectrotemporal processing

Indexed keywords

ARTICLE; AUDITORY STIMULATION; CLINICAL ARTICLE; ELECTROCORTICOGRAPHY; FEMALE; HUMAN; MALE; NEUROMODULATION; NEUROPHYSIOLOGY; PRIORITY JOURNAL; SPATIAL ANALYSIS; SPECTROTEMPORAL PROCESSING; SPEECH PERCEPTION; STIMULUS RESPONSE; SUPERIOR TEMPORAL GYRUS; ADULT; ALGORITHM; BRAIN MAPPING; ENERGY METABOLISM; EVOKED RESPONSE; PHONETICS; PHYSIOLOGY; TEMPORAL LOBE;

ACOUSTIC STIMULATION; ADULT; ALGORITHMS; BRAIN MAPPING; ENERGY METABOLISM; EVOKED POTENTIALS; FEMALE; HUMANS; MALE; PHONETICS; SPEECH PERCEPTION; TEMPORAL LOBE;

EID: 84958819082     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1779-15.2016     Document Type: Article

References (69)

1. Atencio CA, Schreiner CE (2012) Spectrotemporal processing in spectral tuning modules of cat primary auditory cortex. PloS One 7:e31537. CrossRef Medline
2. Atencio CA, Sharpee TO, Schreiner CE (2008) Cooperative nonlinearities in auditory cortical neurons. Neuron 58:956-966. CrossRef Medline
3. Baumann S, Griffiths TD, Sun L, Petkov CI, Thiele A, Rees A (2011) Orthogonal representation of sound dimensions in the primate midbrain. Nat Neurosci 14:423-425. CrossRef Medline
4. Baumann S, Joly O, Rees A, Petkov CI, Sun L, Thiele A, Griffiths TD (2015) The topography of frequency and time representation in primate auditory cortices. Elife 4. CrossRef Medline
5. Binder JR, Rao SM, Hammeke TA, Frost JA, Bandettini PA, Hyde JS (1994) Effects of stimulus rate on signal response during functional magnetic resonance imaging of auditory cortex. Brain Res Cogn Brain Res 2:31-38. CrossRef Medline
6. 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. CrossRef Medline
7. Boatman D (2004) Cortical bases of speech perception: evidence from functional lesion studies. Cognition 92:47-65. CrossRef Medline
8. Boatman D, Hall C, Goldstein MH, Lesser R, Gordon B (1997) Neuroperceptual differences in consonant and vowel discrimination: as revealed by direct cortical electrical interference. Cortex 33:83-98. CrossRef Medline
9. Brenner N, Bialek W, de Ruyter van Steveninck R (2000) Adaptive rescaling maximizes information transmission. Neuron 26:695-702. CrossRef Medline
10. Calabrese A, Schumacher JW, Schneider DM, Paninski L, Woolley SM (2011) A generalized linear model for estimating spectrotemporal receptive fields from responses to natural sounds. PLoS One 6:e16104. CrossRef Medline
11. Carlson NL, Ming VL, Deweese MR (2012) Sparse codes for speech predict spectrotemporal receptive fields in the inferior colliculus. PLoS Comput Biol 8:e1002594. CrossRef Medline
12. Chang EF, Edwards E, Nagarajan SS, Fogelson N, Dalal SS, Canolty RT, Kirsch HE, Barbaro NM, Knight RT (2011) Cortical spatio-temporal dynamics underlying phonological target detection in humans. J Cogn Neurosci 23:1437-1446. CrossRef Medline
13. Crone NE, Boatman D, Gordon B, Hao L (2001) Induced electrocorticographic gamma activity during auditory perception. Brazier Awardwinning article, 2001. Clin Neurophys 112:565-582. CrossRef Medline
14. Dan Y, Atick JJ, Reid RC (1996) Efficient coding of natural scenes in the lateral geniculate nucleus: experimental test of a computational theory. J Neurosci 16:3351-3362. Medline
15. David SV, Vinje WE, Gallant JL (2004) Natural stimulus statistics alter thereceptive field structure of v1 neurons. J Neurosci 24:6991-7006. CrossRef Medline
16. David SV, Mesgarani N, Shamma SA (2007) Estimating sparse spectrotemporal receptive fields with natural stimuli. Network 18:191-212. CrossRef Medline
17. Depireux DA, Simon JZ, Klein DJ, Shamma SA (2001) Spectro-temporal response field characterization with dynamic ripples in ferret primary auditory cortex. J Neurophysiol 85:1220-1234. Medline
18. Dong D, Atick J (1995) Temporal decorrelation: a theory of lagged and nonlagged responses in the lateral geniculate nucleus. Netw Comput Neural Syst 6:159-178. CrossRef
19. Edwards E, Chang EF (2013) Syllabic (~2-5 Hz) and fluctuation (~1-10 Hz) ranges in speech and auditory processing. Hear Res 305:113-134. CrossRef Medline
20. Eggermont JJ (2002) Temporal modulation transfer functions in cat primary auditory cortex: separating stimulus effects from neural mechanisms. J Neurophysiol 87:305-321. Medline
21. Elliott TM, Theunissen FE (2009) The modulation transfer function for speech intelligibility. PLoS Comput Biol 5:e1000302. CrossRef Medline
22. Escabi MA, Schreiner CE (2002) Nonlinear spectrotemporal sound analysis by neurons in the auditory midbrain. J Neurosci 22:4114-4131. Medline
23. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck RR (2001) Efficiency and ambiguity in an adaptive neural code. Nature 412:787-792. CrossRef Medline
24. Felsen G, Touryan J, Han F, Dan Y (2005) Cortical sensitivity to visual features in natural scenes. PLoS Biol 3:e342. CrossRef Medline
25. Garofolo J, Lamel LF, Fisher WM, Fiscus J, Pallett D, Dahlgren N, Zue V (1993) TIMIT acoustic-phonetic continuous speech corpus. Philadelphia: Linguistic Data Consortium.
26. Gross J, Hoogenboom N, Thut G, Schyns P, Panzeri S, Belin P, Garrod S (2013) Speech rhythms and multiplexed oscillatory sensory coding in the human brain. PLoS Biol 11:e1001752. CrossRef Medline
27. Harms MP, Melcher JR (2002) Sound repetition rate in the human auditory pathway: representations in the waveshape and amplitude of fMRI activation. J Neurophysiol 88:1433-1450. Medline
28. Herdener M, Esposito F, Scheffler K, Schneider P, Logothetis NK, Uludag K, Kayser C (2013) Spatial representations of temporal and spectral sound cues in human auditory cortex. Cortex 49:2822-2833. CrossRef Medline
29. Hickok G, Poeppel D (2007) The cortical organization of speech processing. Nat Rev Neurosci 8:393-402. CrossRef Medline
30. Hsu A, Woolley SM, Fremouw TE, Theunissen FE (2004) Modulation power and phase spectrum of natural sounds enhance neural encoding performed by single auditory neurons. J Neurosci 24:9201-9211. CrossRef Medline
31. Kim G, Doupe A (2011) Organized representation of spectrotemporal features in songbird auditory forebrain. J Neurosci 31:16977-16990. CrossRef Medline
32. Klein DJ, Depireux DA, Simon JZ, Shamma SA (2000) Robust spectrotemporal reverse correlation for the auditory system: optimizing stimulus design. J Comput Neurosci 9:85-111. CrossRef Medline
33. Klein DJ, Simon JZ, Depireux DA, Shamma SA (2006) Stimulus-invariant processing and spectrotemporal reverse correlation in primary auditory cortex. J Comput Neurosci 20:111-136. CrossRef Medline
34. Langers DR, Backes WH, van Dijk P (2003) Spectrotemporal features of the auditory cortex: the activation in response to dynamic ripples. Neuroimage 20:265-275. CrossRef Medline
35. Liégeois-Chauvel C, Lorenzi C, Trébuchon A, Régis J, Chauvel P (2004) Temporal envelope processing in the human left and right auditory cortices. Cereb Cortex 14:731-740. CrossRef Medline
36. Malone BJ, Scott BH, Semple MN (2007) Dynamic amplitude coding in the auditory cortex of awake rhesus macaques. J Neurophysiol 98:1451-1474. CrossRef Medline
37. Malone BJ, Beitel RE, Vollmer M, Heiser MA, Schreiner CE (2013) Spectral context affects temporal processing in awake auditory cortex. J Neurosci 33:9431-9450. CrossRef Medline
38. McDermott JH, Simoncelli EP (2011) Sound texture perception via statistics of the auditory periphery: evidence from sound synthesis. Neuron 71:926-940. CrossRef Medline
39. Miller LM, Escabí MA, Read HL, Schreiner CE (2002) Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. J Neurophysiol 87:516-527. Medline
40. Moerel M, De Martino F, Formisano E (2012) Processing of natural sounds in human auditory cortex: tonotopy, spectral tuning, and relation to voice sensitivity. J Neurosci 32:14205-14216. CrossRef Medline
41. Nagel KI, Doupe AJ (2008) Organizing principles of spectro-temporal encoding in the avian primary auditory area field L. Neuron 58:938-955. CrossRef Medline
42. Nourski KV, Steinschneider M, Oya H, Kawasaki H, Jones RD, Howard MA (2014) Spectral organization of the human lateral superior temporal gyrus revealed by intracranial recordings. Cereb Cortex 24:340-352. CrossRef Medline
43. Olshausen BA, Field DJ (1996) Emergence of simple-cell receptive field properties by learning a sparse code for natural images. Nature 381:607-609. CrossRef Medline
44. Overath T, Zhang Y, Sanes DH, Poeppel D (2012) Sensitivity to temporal modulation rate and spectral bandwidth in the human auditory system: fMRI evidence. J Neurophysiol 107:2042-2056. CrossRef Medline
45. Overath T, McDermott JH, Zarate JM, Poeppel D (2015) The cortical analysis of speech-specific temporal structure revealed by responses to sound quilts. Nat Neurosci 18:903-911. CrossRef Medline
46. Paninski L (2004) Maximum likelihood estimation of cascade pointprocess neural encoding models. Network 15:243-262. CrossRef Medline
47. 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. CrossRef Medline
48. Rauschecker JP, Scott SK (2009) Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat Neurosci 12:718-724. CrossRef Medline
49. Ray S, Maunsell JH (2011) Different origins of gamma rhythm and highgamma activity in macaque visual cortex. PLoS Biol 9:e1000610. CrossRef Medline
50. Rieke F, Bodnar DA, Bialek W (1995) Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents. Proc Biol Sci 262:259-265. CrossRef Medline
51. Rinne T, Pekkola J, Degerman A, Autti T, Jääskeläinen IP, Sams M, Alho K (2005) Modulation of auditory cortex activation by sound presentation rate and attention. Hum Brain Mapp 26:94-99. CrossRef Medline
52. Rodríguez FA, Read HL, Escabí MA (2010) Spectral and temporal modulation tradeoff in the inferior colliculus. J Neurophysiol 103:887-903. CrossRef Medline
53. Santoro, R, Moerel, M, De Martino, F, Goebel, R, Ugurbil, K, Yacoub, E, and Formisano, E (2014) Encoding of natural sounds at multiple spectral and temporal resolutions in the human auditory cortex. PLoS Comp Biol 10:e1003412. CrossRef Medline
54. Schönwiesner M, Zatorre RJ (2009) Spectro-temporal modulation transfer function of single voxels in the human auditory cortex measured with high-resolution fMRI. Proc Nat Acad Sci USA 106:14611-14616. CrossRef Medline
55. Schreiner CE, Langner G (1988) Periodicity coding in the inferior colliculus of the cat. II. Topographical organization. J Neurophysiol 60:1823-1840. Medline
56. Sharpee T, Rust NC, Bialek W (2004) Analyzing neural responses to natural signals: maximally informative dimensions. Neural Comput 16:223-250. CrossRef Medline
57. Sharpee TO, Sugihara H, Kurgansky AV, Rebrik SP, Stryker MP, Miller KD (2006) Adaptive filtering enhances information transmission in visual cortex. Nature 439:936-942. CrossRef Medline
58. Smirnakis SM, Berry MJ, Warland DK, Bialek W, Meister M (1997) Adaptation of retinal processing to image contrast and spatial scale. Nature 386:69-73. CrossRef Medline
59. Steinschneider M, Fishman YI, Arezzo JC (2008) Spectrotemporal analysis of evoked and induced electroencephalographic responses in primary auditory cortex (A1) of the awake monkey. Cereb Cortex 18:610-625. CrossRef Medline
60. Striem-Amit E, Hertz U, Amedi A (2011) Extensive cochleotopic mapping of human auditory cortical fields obtained with phase-encoding FMRI. PloS One 6:e17832. CrossRef Medline
61. Talavage TM, Sereno MI, Melcher JR, Ledden PJ, Rosen BR, Dale AM (2004) Tonotopic organization in human auditory cortex revealed by progressions of frequency sensitivity. J Neurophysiol 91:1282-1296. Medline
62. Talebi V, Baker CL Jr (2012) Natural versus synthetic stimuli for estimating receptive field models: a comparison of predictive robustness. J Neurosci 32:1560-1576. CrossRef Medline
63. Tanaka H, Fujita N, Watanabe Y, Hirabuki N, Takanashi M, Oshiro Y, Nakamura H (2000) Effects of stimulus rate on the auditory cortex using fMRI with “sparse” temporal sampling. Neuroreport 11:2045-2049. CrossRef Medline
64. Theunissen FE, Sen K, Doupe AJ (2000) Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J Neurosci 20:2315-2331. Medline
65. 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. CrossRef Medline
66. Wang Y, Ding N, Ahmar N, Xiang J, Poeppel D, Simon JZ (2012) Sensitivity to temporal modulation rate and spectral bandwidth in the human auditory system: MEG evidence. J Neurophysiol 107:2033-2041. CrossRef Medline
67. Wilkinson F, James TW, Wilson HR, Gati JS, Menon RS, Goodale MA (2000) An fMRI study of the selective activation of human extrastriate form vision areas by radial and concentric gratings. Curr Biol 10:1455-1458. CrossRef Medline
68. Yang X, Wang K, Shamma SA (1992) Auditory representations of acoustic signals. IEEE Trans Information Theory 38:824-839. CrossRef
69. Zheng Y, Escabí MA (2008) Distinct roles for onset and sustained activity in the neuronal code for temporal periodicity and acoustic envelope shape. J Neurosci 28:14230-14244. CrossRef Medline