Experimental Brain Research

, Volume 185, Issue 1, pp 11–20 | Cite as

Asynchrony from synchrony: long-range gamma-band neural synchrony accompanies perception of audiovisual speech asynchrony

  • Sam M. Doesburg
  • Lauren L. Emberson
  • Alan Rahi
  • David Cameron
  • Lawrence M. Ward
Research Article

Abstract

Real-world speech perception relies on both auditory and visual information that fall within the tolerated range of temporal coherence. Subjects were presented with audiovisual recordings of speech that were offset by either 30 or 300 ms, leading to perceptually coherent or incoherent audiovisual speech, respectively. We provide electroencephalographic evidence of a phase-synchronous gamma-oscillatory network that is transiently activated by the perception of audiovisual speech asynchrony, showing both topological and time–course correspondence to networks reported in previous neuroimaging research. This finding addresses a major theoretical hurdle regarding the mechanism by which distributed networks serving a common function achieve transient functional integration. Moreover, this evidence illustrates an important dissociation between phase-synchronization and stimulus coherence, highlighting the functional nature of network-based synchronization.

Keywords

EEG Neural synchronization Gamma Multimodal speech Integration 

Supplementary material

221_2007_1127_MOESM1_ESM.doc (1.1 mb)
(DOC 1163 kb)

References

  1. Bushara KO, Grafman J, Hallet M (2001) Neural correlates of auditory-visual stimulus onset asynchrony. J Neurosci 21(1):300–304PubMedGoogle Scholar
  2. Callan DE, Callan AM, Kroos C, Vatikiotis-Bateson E (2001) Multimodal contribution to speech perception revealed by independent component analysis: a single-sweep EEG case study. Cog Brain Res 10:349–353CrossRefGoogle Scholar
  3. Calvert GA, Campbell R, Brammer MJ (2000) Evidence from functional magnetic resonance imaging of crossmodal binding in human heteromodal cortex. Curr Biol 10:649–657PubMedCrossRefGoogle Scholar
  4. Calvert GA (2001) Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cer Cortex 11:1110–1123CrossRefGoogle Scholar
  5. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsh HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in the human neocortex. Science 313:1626–1628PubMedCrossRefGoogle Scholar
  6. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics. J Neurosci Methods 134:9–21PubMedCrossRefGoogle Scholar
  7. Dixon NF, Spitz L (1980) The detection of auditory visual desynchrony. Perception 9:719–721PubMedCrossRefGoogle Scholar
  8. Doesburg SM, Kitajo K, Ward LM (2005) Increased gamma-band synchrony precedes switching of conscious perceptual objects in binocular rivalry. Neuroreport 2:229–239Google Scholar
  9. Eggermont JJ (2000) Sound-induced synchronization of neural activity between and within three cortical areas. J Neurophysiol 83:2708–2722PubMedGoogle Scholar
  10. Engel AK, Singer W (2001) Temporal binging and the neural correlates of sensory awareness. Trends Cogn Sci 5:16–25PubMedCrossRefGoogle Scholar
  11. Fingelkurts AA, Fingelkurts AA, Krause CM, Möttönen R, Sams M (2003) Cortical operational synchrony during audio–visual speech integration. Brain Lang 85:297–312PubMedCrossRefGoogle Scholar
  12. Ford JM, Gray M, Faustman WO, Heinks, Mathalon DH (2005) Reduced gamma-band coherence to distorted feedback during speech when what you say is not what you hear. Int J Psychophysiol 57:143–150PubMedCrossRefGoogle Scholar
  13. Freeman WJ (2004) Origin, structure, and role of background EEG activity. Part 1. Analytic amplitude. Clin Neurophysiol 115:2077–2088PubMedCrossRefGoogle Scholar
  14. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–479PubMedCrossRefGoogle Scholar
  15. Grossberg S (1995) The attentive brain. Am Sci 83:483–449Google Scholar
  16. Jones JA, Callan DE (2003) Brain activity during audiovisual speech perception: an fMRI study of the McGurk effect. Neuroreport 14(8):1129–1133PubMedCrossRefGoogle Scholar
  17. Kaiser J, Hertrich I, Ackermann H, Lutzenberger W (2006) Gamma-band activity over early sensory areas predicts detection of changes in audiovisual speech stimuli. Neuroimage 15:646–653Google Scholar
  18. Kaiser J, Hertrich I, Ackermann H, Mathiak K, Lutzenberger W (2005) Hearing lips: gamma-band activity during audiovisual speech perception. Cer Cortex 15:646–653CrossRefGoogle Scholar
  19. Kanayama N, Sato A, Ohira H (2007) Crossmodal effect with rubber hand illusion and gamma-band activity. Psychophysiol 44: 392–402CrossRefGoogle Scholar
  20. King AJ (2005) Multisensory integration: strategies for synchronization. Curr Biol 15(9):R339–R341PubMedCrossRefGoogle Scholar
  21. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ (1999) Measuring phase synchrony in brain signals. Hum Brain Mapp 8(4):94–208CrossRefGoogle Scholar
  22. Lewkowicz DJ (1996) Perception of auditory–visual temporal synchrony in human infants. J Exp Psychol: Hum Percept Perform 22(5):1194–1106Google Scholar
  23. McGurk H, MacDonald J (1975) Hearing lips and seeing voices. Nature 264:746–748CrossRefGoogle Scholar
  24. Miller LM, D’Esposito M (2005) Perceptual fusion and stimulus coincidence in the cross-modal integration of speech. J Neurosci 25(25):5884–5893PubMedCrossRefGoogle Scholar
  25. Perrin F, Bertrand O, Pernier J (1987) Scalp current density mapping: value and estimation from potential data. IEEE Trans Biomed Eng BME 34:283–288CrossRefGoogle Scholar
  26. Pikovski A, Rosenblum M, Kurths J (2001) Synchronization: a universal concept in nonlinear sciences. Cambridge University Press, Cambridge 432 pGoogle Scholar
  27. Rodriguez E, George N, Lachaux JP, Martinirie J, Renault B, Varela FJ (1999) Perception’s shadow: long-distance synchronization of human brain activity. Nature 397:430–433PubMedCrossRefGoogle Scholar
  28. Schroeder E, Foxe J (2005) Multisensory contributions to low-level “unisensory” processing. Curr Opin Neurobiol 6(4):285–296Google Scholar
  29. Senkowski D, Talsma D, Grigutsch M, Herrmann CS, Woldorff M (2007) Good times for multisensory integration: effects of the precision of temporal synchrony as revealed by gamma-band oscialltions. Neuropsychologia 45(3):561–571PubMedCrossRefGoogle Scholar
  30. Senkowski D, Talsma D, Herrmann CS, Woldorff M (2005) Multisensory processing and oscillatory gamma responses: effects of spatial selective attention. Exp Brain Res 166:411–426PubMedCrossRefGoogle Scholar
  31. Shadlen MN, Movshon JA (1999) Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 24:67–77PubMedCrossRefGoogle Scholar
  32. Tallon-Baudry C, Bertrand O (1999) Oscillatory gamma activity in human and its role in object representation. Trends Cogn Sci 3(4):151–162PubMedCrossRefGoogle Scholar
  33. Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2(4):229–239PubMedCrossRefGoogle Scholar
  34. von Stein A, Sarnthein J (2000) Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta. Int J Psychophysiol 38(3):301–313PubMedCrossRefGoogle Scholar
  35. Ward LM (2003) Synchronous neural oscillations and cognitive processes. Trends Cogn Sci 17:553–559CrossRefGoogle Scholar
  36. Wright TM, Pelphrey KA, Allison T, McKeown MJ, McCarthy G (2003) Polysensory interaction along temporal regions evoked by audiovisual speech. Cer Cortex 13:1034–1043CrossRefGoogle Scholar
  37. Yuval-Greenberg S, Deouell LY (2007) What you see is not (always) what you hear: induced gamma band responses reflect cross-modal interactions in familiar object recognition. J Neurosci 27(5):1090–1096PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Sam M. Doesburg
    • 1
  • Lauren L. Emberson
    • 1
    • 3
  • Alan Rahi
    • 1
  • David Cameron
    • 1
  • Lawrence M. Ward
    • 1
    • 2
  1. 1.Psychophysics and Cognitive Neuroscience Laboratory, Department of PsychologyUniversity of British ColumbiaVancouverCanada
  2. 2.The Brain Research CentreUniversity of British ColumbiaVancouverCanada
  3. 3.Cognitive Neuroscience Lab, Department of PsychologyCornell UniversityNew YorkUSA

Personalised recommendations