Parametric merging of MEG and fMRI reveals spatiotemporal differences in cortical processing of spoken words and environmental sounds in background noise

Cerebral Cortex

Volumn 22, Issue 1, 2012, Pages 132-143

  Renvall, Hanna ^a,b   Formisano, Elia ^a   Parviainen, Tiina ^b,c   Bonte, Milene ^a   Vihla, Minna ^b   Salmelin, Riitta ^b  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b AALTO UNIVERSITY   (Finland)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

auditory; multimodal; speech

Indexed keywords

ADULT; ARTICLE; AUDITORY CORTEX; BRAIN FUNCTION; CLINICAL ARTICLE; COGNITION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MAGNETOENCEPHALOGRAPHY; MALE; NOISE; PRIORITY JOURNAL;

ACOUSTIC STIMULATION; ADULT; ANALYSIS OF VARIANCE; AUDITORY CORTEX; AUDITORY PERCEPTION; BRAIN MAPPING; ENVIRONMENT; EVOKED POTENTIALS, AUDITORY; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MAGNETOENCEPHALOGRAPHY; MALE; NOISE; OXYGEN; REACTION TIME; SOUND; VOCABULARY;

EID: 84055184562     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr095     Document Type: Article

References (68)

1. Ballas JA, Howard JH, Jr. 1987. Interpreting the language of environmental sounds. Environ Behav. 19:91-114.
2. Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS. 1993. Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med. 30:161-173. (Pubitemid 23223577)
3. Benson RR, Richardson M, Whalen DH, Lai S. 2006. Phonetic processing areas revealed by sinewave speech and acoustically similar nonspeech. Neuroimage. 31:342-353. (Pubitemid 43728979)
4. Benson RR, Whalen DH, Richardson M, Swainson B, Clark VP, Lai S, Liberman AM. 2001. Parametrically dissociating speech and nonspeech perception in the brain using fMRI. Brain Lang. 78:364-396. (Pubitemid 32881116)
5. Billings CJ, Tremblay KL, Stecker GC, Tolin WM. 2009. Human evoked cortical activity to signal-to-noise ratio and absolute signal level. Hear Res. 254:15-24.
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. (Pubitemid 30318458)
7. Boersma P. 1993. Accurate short-term analysis of the fundamental frequency and the harmonic-to-noise ratio of a sampled sound. Proc Inst Phon Sci. 17:97-110.
8. Bonte M, Parviainen T, Hytönen K, Salmelin R. 2006. Time course of top-down and bottom-up influences on syllable processing in the auditory cortex. Cereb Cortex. 16:115-123. (Pubitemid 41746735)
9. Boynton GM, Engel SA, Glover GH, Heeger DJ. 1996. Linear systems analysis of functional magnetic resonance imaging in human V1. J Neurosci. 16:4207-4221. (Pubitemid 26192416)
10. Bradlow AR, Alexander JA. 2007. Semantic and phonetic enhancements for speech-in-noise recognition by native and non-native listeners. J Acoust Soc Am. 121:2339-2349. (Pubitemid 46548432)
11. Brookes M, Gibson A, Hall S, Furlong P, Barnes G, Hillebrand A, Singh K, Holliday I, Francis S, Morris P. 2005. GLM-beamformer method demonstrates stationary field, alpha ERD and gamma ERS colocalisation with fMRI BOLD response in visual cortex. Neuroimage. 26: 302-308. (Pubitemid 40602910)
12. Clarke S, Bellmann A, Meuli RA, Assal G, Steck AJ. 2000. Auditory agnosia and auditory spatial deficits following left hemispheric lesions: evidence for distinct processing pathways. Neuropsychologia. 38:797-807. (Pubitemid 30109458)
13. Cummings A, Čeponiene R, Dick F, Saygin AP, Townsend J. 2008. A developmental ERP study of verbal and non-verbal semantic processing. Brain Res. 1208:137-149.
14. Cummings A, Čeponiene R, Koyama A, Saygin AP, Townsend J, Dick F. 2006. Auditory semantic networks for words and natural sounds. Brain Res. 1115:92-107. (Pubitemid 44436091)
15. Cummings A, Saygin AP, Bates E, Dick F. 2009. Infants' recognition of meaningful verbal and nonverbal sounds. Lang Learn Dev. 5:172-190.
16. Cunningham J, Nicol T, Zecker SG, Bradlow A, Kraus N. 2001. Neurobiologic responses to speech in noise in children with learning problems: deficits and strategies for improvement. Clin Neurophysiol. 112:758-767. (Pubitemid 32406250)
17. 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.
18. Davis MH, Johnsrude I. 2003. Hierarchical processing in spoken language comprehension. J Neurosci. 23:3423-3431. (Pubitemid 36531984)
19. Dick F, Saygin AP, Galati G, Pitzalis S, Bentrovato S, D'Amico S, Wilson S, Bates E, Pizzamiglio L. 2007. What is involved and what is necessary for complex linguistic and nonlinguistic auditory processing: evidence from functional magnetic resonance imaging and lesion data. J Cogn Neurosci. 19:799-816. (Pubitemid 46740448)
20. Formisano E, De Martino F, Bonte M, Goebel R. 2008. "Who" is saying "what" Brain-based decoding of human voice and speech. Science. 322:970-973.
21. Foucher JR, Otzenberger H, Gounot D. 2003. The BOLD response and the gamma oscillations respond differently than evoked potentials: an interleaved EEG-fMRI study. BMC Neurosci. 4:22.
22. Goebel R, Esposito F, Formisano E. 2006. Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from singlesubject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum Brain Mapp. 27:392-401. (Pubitemid 43787637)
23. Gygi B, Kidd GR, Watson CS. 2004. Spectral-temporal factors in the identification of environmental sounds. J Acoust Soc Am. 115:1252-1265. (Pubitemid 38298575)
24. Hämäläinen M, Hari R, Ilmoniemi RJ, Knuutila J, Lounasmaa OV. 1993. Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev Mod Phys. 65:413-497.
25. Hari R. 1990. The neuromagnetic method in the study of the human auditory cortex. In: Grandori F, Hoke M, Romani GL, editors. Auditory Evoked Magnetic Fields and Electric Potentials. Basel (Switzerland): Karger. p. 222-282.
26. Helenius P, Salmelin R, Service E, Connolly J, Leinonen S, Lyytinen H. 2002. Cortical activation during spoken-word segmentation in nonreading-impaired and dyslexic adults. J Neurosci. 22:2936-2944. (Pubitemid 37465842)
27. Jäncke L, Wüstenberg T, Scheich H, Heinze HJ. 2002. Phonetic perception and the temporal cortex. Neuroimage. 15:733-746. (Pubitemid 34852490)
28. Kaplan-Neeman R, Kishon-Rabin L, Henkin Y, Muchnik C. 2006. Identification of syllables in noise: electrophysiological and behavioral correlates. J Acoust Soc Am. 120:926-933. (Pubitemid 44213704)
29. Korvenoja A, Huttunen J, Salli E, Pohjonen H, Martinkauppi S, Palva JM, Lauronen L, Virtanen J, Ilmoniemi RJ, Aronen HJ. 1999. Activation of multiple cortical areas in response to somatosensory stimulation: combined magnetoencephalographic and functional magnetic resonance imaging. Hum Brain Mapp. 8:13-27. (Pubitemid 29323846)
30. Kozou H, Kujala T, Shtyrov Y, Toppila E, Starck J, Alku P, Näätänen R. 2005. The effect of different noise types on the speech and nonspeech elicited mismatch negativity. Hear Res. 199:31-39. (Pubitemid 39582777)
31. Lewis JW, Brefczynski JA, Phinney RE, Janik JJ, DeYoe EA. 2005. Distinct cortical pathways for processing tool versus animal sounds. J Neurosci. 25:5148-5158. (Pubitemid 40726968)
32. 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.
33. Liebenthal E, Binder JR, Spitzer SM, Possing ET, Medler DA. 2005. Neural substrates of phonemic perception. Cereb Cortex. 15:1621-1631. (Pubitemid 41344511)
34. Martin BA, Kurtzberg D, Stapells D. 1999. The effects of decreased audibility produced by high-pass noise masking on N1 and the mismatch negativity to speech sounds /ba/and /da/. J Speech Lang Hear Res. 42:271-286. (Pubitemid 29174432)
35. Martin BA, Sigal A, Kurtzberg D, Stapells DR. 1997. The effect of decreasing audibility produced by high-pass noise masking on cortical event-related potentials to speech sounds /ba/and /da/. J Acoust Soc Am. 101:1585-1599. (Pubitemid 27114263)
36. Martin BA, Stapells DR. 2005. Effects of low-pass noise masking on auditory event-related potentials to speech. Ear Hear. 26:195-213. (Pubitemid 40489329)
37. Müller-Gass A, Marcoux A, Logan J, Campbell K. 2001. The intensity of masking noise affects the mismatch negativity to speech sounds in human subjects. Neurosci Lett. 299:197-200. (Pubitemid 32124845)
38. Näätänen R, Lehtokoski A, Lennes M, Cheour M, Huotilainen M, Iivonen A, Vainio M, Alku P, Ilmoniemi RJ, Luuk A, et al. 1997. Language-specific phoneme representations revealed by electric and magnetic brain responses. Nature. 385:432-434. (Pubitemid 27065927)
39. 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. (Pubitemid 44078928)
40. Obleser J, Eisner F, Kotz S. 2008. Bilateral speech comprehension reflects differential sensitivity to spectral and temporal features. J Neurosci. 28:8116-8124.
41. Obleser J, Lahiri A, Eulitz C. 2004. Magnetic brain response mirrors extraction of phonological features from spoken vowels. J Cogn Neurosci. 16:31-39. (Pubitemid 38117584)
42. Okamoto H, Stracke H, Wolters CH, Schmael F, Pantev C. 2007. Attention improves population-level frequency tuning in human auditory cortex. J Neurosci. 27:10383-10390. (Pubitemid 47502002)
43. Parbery-Clark A, Skoe E, Kraus N. 2009. Musical experience limits the degradative effects of background noise on the neural processing of sound. J Neurosci. 29:14100-14107.
44. Poeppel D, Yellin E, Phillips C, Roberts TP, Rowley HA, Wexler K, Marantz A. 1996. Task-induced asymmetry of the auditory evoked M100 neuromagnetic field elicited by speech sounds. Brain Res Cogn Brain Res. 4:231-242. (Pubitemid 26390782)
45. Price C, Thierry G, Griffiths T. 2005. Speech-specific auditory processing: where is it Trends Cogn Sci. 9:271-276.
46. Raij T, Ahveninen J, Lin F, Witzel T, Jääskeläinen I, Letham B, Israeli E, Sahyoun C, Vasios C, Stufflebeam S, et al. 2010. Onset timing of cross-sensory activations and multisensory interactions in auditory and visual sensory cortices. Eur J Neurosci. 31:1772-1782.
47. Riecke L, van Opstal AJ, Goebel R, Formisano E. 2007. Hearing illusory sounds in noise: sensory-perceptual transformations in primary auditory cortex. J Neurosci. 27:12684-12689. (Pubitemid 350127824)
48. Riede T, Herzel H, Hammerschmidt K, Brunnberg L, Tembrock G. 2001. The harmonic-to-noise ratio applied to dog barks. J Acoust Soc Am. 110:2191-2197. (Pubitemid 32959717)
49. Salmelin R. 2007. Clinical neurophysiology of language: the MEG approach. Clin Neurophysiol. 118:237-254. (Pubitemid 46038804)
50. Saygin A, Dick F, Wilson S, Dronkers N, Bates E. 2003. Neural resources for processing language and environmental sounds. Evidence from aphasia. Brain. 126:928-945. (Pubitemid 36372990)
51. Schnider A, Benson DF, Alexander DN, Schnider-Klaus A. 1994. Nonverbal environmental sound recognition after unilateral hemispheric stroke. Brain. 117:281-287. (Pubitemid 24155500)
52. Scott SK, Blank CC, Rosen S, Wise RJ. 2000. Identification of a pathway for intelligible speech in the left temporal lobe. Brain. 123:2400-2406.
53. Scott SK, Rosen S, Wickham L, Wise RJS. 2004. A positron emission tomography study of the neural basis of informational and energetic masking effects in speech perception. J Acoust Soc Am. 115:813-821. (Pubitemid 38200667)
54. Seither-Preisler A, Krumbholz K, Lütkenhöner B. 2003. Sensitivity of the neuromagnetic N100m deflection to spectral bandwidth: a function of the auditory periphery Audiol Neurotol. 8:322-337. (Pubitemid 37336445)
55. Shah NJ, Steinhoff S, Mirzazade S, Zafiris O, Grosse-Ruyken ML, Jäncke L, Zilles K. 2000. The effect of sequence repeat time on auditory cortex stimulation during phonetic discrimination. Neuroimage. 12:100-108. (Pubitemid 30602067)
56. Shahin A, Roberts LE, Pantev C, Trainor LJ, Ross B. 2005. Modulation of P2 auditory evoked responses by the spectral complexity of musical sounds. Neuroreport. 16:1781-1785. (Pubitemid 41547046)
57. Sharon D, Hämä läinen M, Tootell R, Halgren E, Belliveau J. 2007. The advantage of combining MEG and EEG: comparison to fMRI in focally stimulated visual cortex. Neuroimage. 36:1225-1235. (Pubitemid 47008957)
58. Soeta Y, Nakagawa S, Tonoike M. 2005. Auditory evoked magnetic fields in relation to bandwidth variations of bandpass noise. Hear Res. 202:47-54. (Pubitemid 40469769)
59. Staeren N, Renvall H, De Martino F, Goebel R, Formisano E. 2009. Sound categories are represented as distributed patterns in the human auditory cortex. Curr Biol. 19:498-502.
60. Stracke H, Okamoto H, Pantev C. 2009. Interhemispheric support during demanding auditory signal-in-noise processing. Cereb Cortex. 19:1440-1447.
61. Talairach J, Tournoux P. 1988. Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system: an approach to cerebral imaging. New York: Thieme Medical Publishers.
62. Uusvuori J, Parviainen T, Inkinen M, Salmelin R. 2008. Spatiotemporal interaction between sound form and meaning during spoken word perception. Cereb Cortex. 18:456-466.
63. van Atteveldt N, Formisano E, Goebel R, Blomert L. 2004. Integration of letters and speech sounds in the human brain. Neuron. 43:271-282. (Pubitemid 38942966)
64. Van Petten C, Rheinfelder H. 1995. Conceptual relationships between spoken words and environmental sounds: event-related brain potential measures. Neuropsychologia. 33:485-508.
65. Vartiainen J, Liljestrom M, Koskinen M, Renvall H, Salmelin R. 2011. Functional magnetic resonance imaging blood oxygenation leveldependent signal and magnetoencephalography evoked responses yield different neural functionality in reading. J Neurosci. 31:1048-1058.
66. Vouloumanos A, Kiehl KA, Werker JF, Liddle PF. 2001. Detection of sounds in the auditory stream: event-related fMRI evidence for differential activation to speech and nonspeech. J Cogn Neurosci. 13:994-1005. (Pubitemid 32978065)
67. Whiting KA, Martin BA, Stapells DR. 1998. The effects of broadband noise masking on cortical event-related potentials to speech sounds /ba/and /da/. Ear Hear. 19:218-231. (Pubitemid 28285601)
68. Zatorre RJ, Belin P. 2001. Spectral and temporal processing in human auditory cortex. Cereb Cortex. 11:946-953. (Pubitemid 32946228)