Cortical pitch regions in humans respond primarily to resolved harmonics and are located in specific tonotopic regions of anterior auditory cortex

Journal of Neuroscience

Volumn 33, Issue 50, 2013, Pages 19451-19469

  Norman Haignere, Sam ^a,b   Kanwisher, Nancy ^a,b   McDermott, Josh H ^b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Auditory cortex; fMRI; Periodicity; Pitch; Resolved harmonics; Tonotopy

Indexed keywords

ADULT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; AUDITORY SYSTEM PARAMETERS; BEHAVIOR; BRAIN CORTEX; CONTROLLED STUDY; FATIGUE; FEMALE; FOLLOW UP; FREQUENCY VARIATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HARMONICS RESOLVABILITY; HEARING; HUMAN; HUMAN EXPERIMENT; MALE; MEASUREMENT; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; TONOTOPY;

AUDITORY CORTEX; FMRI; PERIODICITY; PITCH; RESOLVED HARMONICS; TONOTOPY;

ACOUSTIC STIMULATION; ADULT; AUDITORY CORTEX; AUDITORY PATHWAYS; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; PITCH DISCRIMINATION; PITCH PERCEPTION;

EID: 84889819597     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2880-13.2013     Document Type: Article

References (84)

1. Barker D, Plack CJ, Hall DA (2011) Human auditory cortical responses to pitch and to pitch strength. Neuroreport 22:111-115. CrossRef Medline
2. Barker D, Plack CJ, Hall DA (2012) Reexamining the evidence for a pitchsensitive region: a human fMRI study using iterated ripple noise. Cereb Cortex 22:745-753. CrossRef Medline
3. Barker D, Plack CJ, Hall DA (2013) Representations of pitch and slow modulation salience in auditory cortex. Front Syst Neurosci 7:62. CrossRef Medline
4. Barrett DJ, Hall DA (2006) Response preferences for "what" and "where" in human non-primary auditory cortex. Neuroimage 32:968-977. CrossRef Medline
5. Baumann S, Petkov CI, Griffiths TD (2013) A unified framework for the organization of auditory cortex. Front Syst Neurosci 7:1-8. CrossRef Medline
6. Bendor D (2012) Does a pitch center exist in auditory cortex? J Neurophysiol 107:743-746. CrossRef Medline
7. Bendor D, Wang X (2005) The neuronal representation of pitch in primate auditory cortex. Nature 436:1161-1165. CrossRef Medline
8. Bendor D, Wang X (2006) Cortical representations of pitch in monkeys and humans. Curr Opin Neurobiol 16:391-399. CrossRef Medline
9. Bendor D, Wang X (2010) The neuronal coding of periodicity in marmoset auditory cortex. J Neurophysiol 103:1809-1822. CrossRef Medline
10. Bendor D, Osmanski MS, Wang X (2012) Dual-pitch processing mechanisms in primate auditory cortex. J Neurosci 32:16149-16161. CrossRef Medline
11. Bernstein JG, Oxenham AJ (2005) An autocorrelation model with place dependence to account for the effect of harmonic number on fundamental frequency discrimination. J Acoust Soc Am 117:3816-3831. CrossRef Medline
12. Bizley JK, Walker KM (2010) Sensitivity and selectivity of neurons in auditory cortex to the pitch, timbre, and location of sounds. Neuroscientist 16:453-469. CrossRef Medline
13. Carlyon RP, Shackleton TM (1994) Comparing the fundamental frequencies of resolved and unresolved harmonics: evidence for two pitch mechanisms. J Acoust Soc Am 95:3541-3554. CrossRef
14. Chait M, Poeppel D, Simon JZ (2006) Neural response correlates of detection of monaurally and binaurally created pitches in humans. Cereb Cortex 16:835-848. CrossRef Medline
15. Da Costa S, van der Zwaag W, Marques JP, Frackowiak RS, Clarke S, SaenzM (2011) Human primary auditory cortex follows the shape of Heschl's gyrus. J Neurosci 31:14067-14075. CrossRef Medline
16. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968-980. CrossRef Medline
17. Dowling WJ (1978) Scale and contour: two components of a theory of memory for melodies. Psychological Review 85:341-354. CrossRef
18. Ellis DPW (2009) Gammatone-like spectrograms. Available from: http:// www.ee.columbia.edu/ln/rosa/matlab/gammatonegram/. Accessed November 15, 2013.
19. Fastl H (1980) Pitch strength and masking patterns of low-pass noise. In: Psychophysical, physiological, and behavioral studies in hearing (Brink GVD, Bilsen F, eds), pp 334-339. Delft, The Netherlands: Delft UP.
20. Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II. Inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195-207. CrossRef Medline
21. Fishman YI, Micheyl C, Steinschneider M (2013) Neural representation of complex tones in primary auditory cortex of the awake monkey. J Neurosci 33:10312-10323. CrossRef Medline
22. Garcia D, Hall DA, Plack CJ (2010) The effect of stimulus context on pitch representations in the human auditory cortex. Neuroimage 51:808-816. CrossRef Medline
23. Glasberg BR, Moore BCJ (1990) Derivation of auditory filter shapes from notched-noise data. Hearing Res 47:103-138. CrossRef Medline
24. Glasberg BR, Moore BC (2006) Prediction of absolute thresholds and equalloudness contours using a modified loudness model. J Acoust Soc Am 120:585-588. CrossRef Medline
25. Goldstein JL (1967) Auditory nonlinearity. J Acoust Soc Am 41:676-689. CrossRef Medline
26. Goldstein JL (1973) An optimum processor theory for the central formation of the pitch of complex tones. J Acoust Soc Am 54:1496-1516. CrossRef Medline
27. Greve DN, Fischl B (2009) Accurate and robust brain image alignment using boundary-based registration. Neuroimage 48:63-72. CrossRef Medline
28. Griffiths TD, Hall DA (2012) Mapping pitch representation in neural ensembles with fMRI. J Neurosci 32:13343-13347. CrossRef Medline
29. Griffiths TD, Büchel C, Frackowiak RS, Patterson RD (1998) Analysis of temporal structure in sound by the human brain. Nat Neurosci 1:422-427. CrossRef Medline
30. Griffiths TD, Kumar S, Sedley W, Nourski KV, Kawasaki H, Oya H, Patterson RD, Brugge JF, HowardMA (2010) Direct recordings of pitch responses from human auditory cortex. Curr Biol 20:1128-1132. CrossRef Medline
31. Gutschalk A, Patterson RD, Rupp A, Uppenkamp S, Scherg M (2002) Sustained magnetic fields reveal separate sites for sound level and temporal regularity in human auditory cortex. Neuroimage 15:207-216. CrossRef Medline
32. Gutschalk A, Patterson RD, Scherg M, Uppenkamp S, Rupp A (2004) Temporal dynamics of pitch in human auditory cortex. Neuroimage 22:755-766. CrossRef Medline
33. Hall DA, Plack CJ (2007) The human 'pitch center' responds differently to iterated noise and Huggins pitch. Neuroreport 18:323-327. CrossRef Medline
34. Hall DA, Plack CJ (2009) Pitch processing sites in the human auditory brain. Cereb Cortex 19:576-585. CrossRef Medline
35. Hall DA, Haggard MP, Akeroyd MA, Palmer AR, Summerfield AQ, Elliott MR, Gurney EM, Bowtell RW (1999) "Sparse" temporal sampling in auditory fMRI. Hum Brain Mapp 7:213-223. CrossRef Medline
36. Hall DA, Barrett DJ, Akeroyd MA, Summerfield AQ (2005) Cortical representations of temporal structure in sound. J Neurophysiol 94:3181-3191. CrossRef Medline
37. Hall DA, Edmondson-Jones AM, Fridriksson J (2006) Periodicity and frequency coding in human auditory cortex. Eur J Neurosci 24:3601-3610. CrossRef Medline
38. Houtsma AJM, Smurzinski J (1990) Pitch identification and discrimination for complex tones with many harmonics. J Acoust Soc Am 87:304-310. CrossRef
39. Humphries C, Liebenthal E, Binder JR (2010) Tonotopic organization of human auditory cortex. Neuroimage 50:1202-1211. CrossRef Medline
40. Jenkinson M (1999) Measuring transformation error by RMS deviation: FMRIB Technical Report. Available from: http://fsl.fmrib.ox.ac.uk/ analysis/techrep/tr99mj1/tr99mj1.pdf. Accessed November 15, 2013.
41. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Medical Image Analysis 5:143-156. CrossRef Medline
42. Krumbholz K, Patterson RD, Seither-Preisler A, Lammertmann C, Lütkenhöner B (2003) Neuromagnetic evidence for a pitch processing center in Heschl's gyrus. Cereb Cortex 13:765-772. CrossRef Medline
43. Lee YS, Janata P, Frost C, Hanke M, Granger R (2011) Investigation of melodic contour processing in the brain using multivariate pattern-based fMRI. Neuroimage 57:293-300. CrossRef Medline
44. Levitt H (1971) Transformed up-down methods in psychoacoustics. J Acoust Soc Am 46:467-477. Medline
45. Lewis JW, Talkington WJ, Walker NA, Spirou GA, Jajosky A, Frum C, Brefczynski-Lewis JA (2009) Human cortical organization for processing vocalizations indicates representation of harmonic structure as a signal attribute. J Neurosci 29:2283-2296. CrossRef Medline
46. Licklider JCR (1954) "Periodicity" pitch and "place" pitch. J Acoust SocAm 26:945. CrossRef Mc
47. Dermott JH, Lehr AJ, Oxenham AJ (2008) Is relative pitch specific to pitch? Psychol Sci 19:1263-1271. CrossRef Medline
48. McDermott JH, Lehr AJ, Oxenham AJ (2010) Individual differences reveal the basis of consonance. Curr Biol 20:1035-1041. CrossRef Medline
49. Meddis R, Hewitt MJ (1991) Virtual pitch and phase sensitivity of a computer model of the auditory periphery. I: Pitch identification. J Acoust Soc Am 89:2866-2882. CrossRef
50. Meyer M, Steinhauer K, Alter K, Friederici AD, von Cramon DY (2004) Brain activity varies with modulation of dynamic pitch variance in sentence melody. Brain Lang 89:277-289. CrossRef Medline
51. Micheyl C, Keebler MV, Oxenham AJ (2010) Pitch perception for mixtures of spectrally overlapping harmonic complex tones. J Acoust Soc Am 128: 257-269. CrossRef Medline
52. 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
53. Moore BC, Huss M, Vickers DA, Glasberg BR, Alcántara JI (2000) A test for the diagnosis of dead regions in the cochlea. Br J Audiol 34:205-224. CrossRef Medline
54. Morosan P, Rademacher J, Schleicher A, Amunts K, Schormann T, Zilles K (2001) Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage 13:684-701. CrossRef Medline
55. Norman KA, Polyn SM, Detre GJ, Haxby JV (2006) Beyond mind-reading: multi-level pattern analysis of fMRI data. Trends Cogn Sci 10:424-430. CrossRef Medline
56. Oxenham AJ (2012) Pitch perception. J Neurosci 32:13335-13338. CrossRef Medline
57. Patterson RD, Robinson JH, McKeown D, Zhang C, Allerhand M (1992) Complex sounds and auditory images. In: Auditory physiology and perception: Proceedings of the 9th International Symposium on Hearing (Cazals Y, Demany L, Horner K, eds), pp 429-446. Oxford: Pergamon.
58. Patterson RD, Uppenkamp S, Johnsrude IS, Griffiths TD (2002) The processing of temporal pitch and melody information in auditory cortex. Neuron 36:767-776. CrossRef Medline
59. Peelle JE, Eason RJ, Schmitter S, Schwarzbauer C, Davis MH (2010) Evaluating an acoustically quiet EPI sequence for use in fMRI studies of speech and auditory processing. Neuroimage 52:1410-1419. CrossRef Medline
60. Penagos H, Melcher JR, Oxenham AJ (2004) A neural representation of pitch salience in nonprimary human auditory cortex revealed with functional magnetic resonance imaging. J Neurosci 24:6810-6815. CrossRef Medline
61. Peretz I, Kolinsky R, Tramo M, Labrecque R, Hublet C, Demeurisse G, Belleville S (1994) Functional dissociations following bilateral lesions of auditory cortex. Brain 117:1283-1301. CrossRef Medline
62. Plack CJ, Oxenham AJ, Fay RR, Popper AN (2005) Pitch: neural coding and perception New York: Springer.
63. Pressnitzer D, Patterson RD (2001) Distortion products and the perceived pitch of harmonic complex tones. In: Physiological and psychophysical bases of auditory function (Breebart DJ, Houtsma AJM, Kohlrausch A, Prijs VF, Schoonoven R, eds), pp 97-104. Maastricht: Shaker Publishing BV.
64. Puschmann S, Uppenkamp S, Kollmeier B, Thiel CM (2010) Dichotic pitch activates pitch processing centre in Heschl's gyrus. Neuroimage 49:1641-1649. CrossRef Medline
65. Schindler A, Herdener M, Bartels A (2013) Coding of melodic gestalt in human auditory cortex. Cereb Cortex 23:2987-2993. CrossRef Medline
66. Schmitter S, Diesch E, Amann M, Kroll A, Moayer M, Schad LR (2008) Silent echoplanar imaging for auditory fMRI. MAGMA 21:317-325. CrossRef Medline
67. Schönwiesner M, Zatorre RJ (2008) Depth electrode recordings show double dissociation between pitch processing in lateral Heschl's Gyrus and sound onset processing in medial Heschl's gyrus. Exp Brain Res 187:97-105. CrossRef Medline
68. Schroeder M (1970) Synthesis of low-peak-factor signals and binary sequences with low autocorrelation. IEEE Transactions on Information Theory 16:85-89. CrossRef
69. Sedley W, Teki S, Kumar S, Overath T, Barnes GR, Griffiths TD (2012) Gamma band pitch responses in human auditory cortex measured with magnetoencephalography. Neuroimage 59:1904-1911. CrossRef Medline
70. Shackleton TM, Carlyon RP (1994) The role of resolved and unresolved harmonics in pitch perception and frequency modulation discrimination. J Acoust Soc Am 95:3529-3540. CrossRef Medline
71. SlaneyM (1998) Auditory toolbox version 2. Interval Research Corporation Technical Report #1998-010. Available from: https://engineering. purdue.edu/~ smalcolm/interval/1998-010/. Accessed November 15, 2013.
72. Small AM Jr, Daniloff RG (1967) Pitch of noise bands. J Acoust Soc Am 41:506-512. CrossRef Medline
73. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, MatthewsPM (2004) Advances in functional and structuralMRimage analysis and implementation as FSL. Neuroimage 23:S208-S219. CrossRef Medline
74. Steinmann I, Gutschalk A (2012) Sustained BOLD and theta activity in auditory cortex are related to slow stimulus fluctuations rather than to pitch. J Neurophysiol 107:3458-3467. CrossRef Medline
75. Stevens CJ (2000) Acoustic phonetics. Cambridge, MA: MIT.
76. 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
77. Terhardt E (1974) Pitch, consonance, and harmony. J Acoust Soc Am 55: 1061-1069. CrossRef Medline
78. Tierney A, Dick F, Deutsch D, Sereno M (2013) Speech versus song: multiple pitch-sensitive areas revealed by a naturally occurring musical illusion. Cereb Cortex 23:249-254. CrossRef Medline
79. Triantafyllou C, Hoge RD, Krueger G, Wiggins CJ, Potthast A, Wiggins GC, Wald LL (2005) Comparison of physiological noise at 1.5 T, 3 T, and 7 T and optimization of fMRI acquisition parameters. Neuroimage 26:243-250. CrossRef Medline
80. Walker KM, Bizley JK, King AJ, Schnupp JW (2011) Multiplexed and robust representations of sound features in auditory cortex. J Neurosci 31: 14565-14576. CrossRef Medline
81. Wang X, WalkerKM (2012) Neural mechanisms for the abstraction and use of pitch information in auditory cortex. J Neurosci 32:13339-13342. CrossRef Medline
82. Warren JD, Griffiths TD (2003) Distinct mechanisms for processing spatial sequences and pitch sequences in the human auditory brain. J Neurosci 23:5799-5804. Medline
83. Woods DL, Stecker GC, Rinne T, Herron TJ, Cate AD, Yund EW, Liao I, Kang X (2009) Functional maps of human auditory cortex: effects of acoustic features and attention. PLoS ONE 4:e5183. CrossRef Medline
84. Zatorre RJ, Belin P, Penhune VB (2002) Structure and function of auditory cortex: music and speech. Trends Cogn Sci 6:37-46. CrossRef Medline