Visual Anticipatory Information Modulates Multisensory Interactions of Artificial Audiovisual Stimuli

The neural activity of speech sound processing (the N1 component of the auditory ERP) can be suppressed if a speech sound is accompanied by concordant lip movements. Here we demonstrate that this audiovisual interaction is neither speech specific nor linked to humanlike actions but can be observed with artificial stimuli if their timing is made predictable. In Experiment 1, a pure tone synchronized with a deformation of a rectangle induced a smaller auditory N1 than auditory-only presentations if the temporal occurrence of this audiovisual event was made predictable by two moving disks that touched the rectangle. Local autoregressive average source estimation indicated that this audiovisual interaction may be related to integrative processing in auditory areas. When the moving disks did not precede the audiovisual stimulus—making the onset unpredictable—there was no N1 reduction. In Experiment 2, the predictability of the leading visual signal was manipulated by introducing a temporal asynchrony between the audiovisual event and the collision of moving disks. Audiovisual events occurred either at the moment, before (too “early”), or after (too “late”) the disks collided on the rectangle. When asynchronies varied from trial to trial—rendering the moving disks unreliable temporal predictors of the audiovisual event—the N1 reduction was abolished. These results demonstrate that the N1 suppression is induced by visual information that both precedes and reliably predicts audiovisual onset, without a necessary link to human action-related neural mechanisms.

[1]  P. Bertelson,et al.  Recalibration of temporal order perception by exposure to audio-visual asynchrony. , 2004, Brain research. Cognitive brain research.

[2]  Sonja A. Kotz,et al.  The temporal dynamics of processing emotions from vocal, facial, and bodily expressions , 2011, NeuroImage.

[3]  Mikko Sams,et al.  Processing of audiovisual speech in Broca's area , 2005, NeuroImage.

[4]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. II. Demonstration of Sublobar Accuracy in Patients with Simultaneous Surface and Depth Recordings , 2004, Brain Topography.

[5]  J. Mazziotta,et al.  Modulation of motor and premotor activity during imitation of target-directed actions. , 2002, Cerebral cortex.

[6]  M. Sams,et al.  Time course of multisensory interactions during audiovisual speech perception in humans: a magnetoencephalographic study , 2004, Neuroscience Letters.

[7]  J. Vroomen,et al.  Perception of intersensory synchrony in audiovisual speech: Not that special , 2011, Cognition.

[8]  Klucharev Vasily,et al.  Electrophysiological indicators of phonetic and non-phonetic multisensory interactions during audiovisual speech perception. , 2003 .

[9]  J. Decety,et al.  The effects of learning and intention on the neural network involved in the perception of meaningless actions. , 1999, Brain : a journal of neurology.

[10]  R. Hari,et al.  Seeing speech: visual information from lip movements modifies activity in the human auditory cortex , 1991, Neuroscience Letters.

[11]  A. Fort,et al.  Bimodal speech: early suppressive visual effects in human auditory cortex , 2004, The European journal of neuroscience.

[12]  Joost X. Maier,et al.  Multisensory Integration of Dynamic Faces and Voices in Rhesus Monkey Auditory Cortex , 2005 .

[13]  M Di Luca,et al.  Recalibration of audiovisual simultaneity , 2010 .

[14]  John J. Foxe,et al.  Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. , 2002, Brain research. Cognitive brain research.

[15]  J. MacDonald,et al.  Hearing Lips and Seeing Voices: Illusion and Serendipity in Auditory‐Visual Perception Research , 2008 .

[16]  C. Spence,et al.  Audiotactile interactions in temporal perception , 2011, Psychonomic bulletin & review.

[17]  Jeffery A. Jones,et al.  Neural processes underlying perceptual enhancement by visual speech gestures , 2003, Neuroreport.

[18]  John J. Foxe,et al.  Multisensory processing of naturalistic objects in motion: A high-density electrical mapping and source estimation study , 2007, NeuroImage.

[19]  John J. Foxe,et al.  Multisensory processing in children with autism: high‐density electrical mapping of auditory–somatosensory integration , 2010, Autism research : official journal of the International Society for Autism Research.

[20]  Marty G. Woldorff,et al.  Selective Attention and Multisensory Integration: Multiple Phases of Effects on the Evoked Brain Activity , 2005, Journal of Cognitive Neuroscience.

[21]  Riitta Hari,et al.  Audiovisual Integration of Letters in the Human Brain , 2000, Neuron.

[22]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[23]  D. Poeppel,et al.  Temporal window of integration in auditory-visual speech perception , 2007, Neuropsychologia.

[24]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[25]  E. Schafer,et al.  Self-Stimulation Alters Human Sensory Brain Responses , 1973, Science.

[26]  I. Peretz,et al.  Born to dance but beat deaf: A new form of congenital amusia , 2011, Neuropsychologia.

[27]  J. Pernier,et al.  Early auditory-visual interactions in human cortex during nonredundant target identification. , 2002, Brain research. Cognitive brain research.

[28]  John J. Foxe,et al.  Multisensory visual-auditory object recognition in humans: a high-density electrical mapping study. , 2004, Cerebral cortex.

[29]  D. Wolpert,et al.  Why can't you tickle yourself? , 2000, Neuroreport.

[30]  A. Brancucci,et al.  Neuromagnetic responses reveal the cortical timing of audiovisual synchrony , 2011, Neuroscience.

[31]  Steven L. Small,et al.  Listening to talking faces: motor cortical activation during speech perception , 2005, NeuroImage.

[32]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[33]  E. Bullmore,et al.  Response amplification in sensory-specific cortices during crossmodal binding. , 1999, Neuroreport.

[34]  David Poeppel,et al.  Visual speech speeds up the neural processing of auditory speech. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Pernier,et al.  Dynamics of cortico-subcortical cross-modal operations involved in audio-visual object detection in humans. , 2002, Cerebral cortex.

[36]  K. Crowley,et al.  A review of the evidence for P2 being an independent component process: age, sleep and modality , 2004, Clinical Neurophysiology.

[37]  Tobias S. Andersen,et al.  Multistage audiovisual integration of speech: dissociating identification and detection , 2011, Experimental Brain Research.

[38]  E Donchin,et al.  The effects of temporal and event uncertainty in determining the waveforms of the auditory event related potential (ERP). , 1976, Psychophysiology.

[39]  Jeffery A. Jones,et al.  Multisensory Integration Sites Identified by Perception of Spatial Wavelet Filtered Visual Speech Gesture Information , 2004, Journal of Cognitive Neuroscience.

[40]  Micah M. Murray,et al.  Auditory–visual multisensory interactions attenuate subsequent visual responses in humans , 2007, NeuroImage.

[41]  K G Munhall,et al.  Audiovisual gating and the time course of speech perception. , 1998, The Journal of the Acoustical Society of America.

[42]  Klaus Scheffler,et al.  Differential patterns of multisensory interactions in core and belt areas of human auditory cortex , 2006, NeuroImage.

[43]  B. Stein,et al.  The Merging of the Senses , 1993 .

[44]  T. Sejnowski,et al.  Early Cross-Modal Interactions in Auditory and Visual Cortex Underlie a Sound-Induced Visual Illusion , 2007, The Journal of Neuroscience.

[45]  Chris I. Baker,et al.  Integration of Visual and Auditory Information by Superior Temporal Sulcus Neurons Responsive to the Sight of Actions , 2005, Journal of Cognitive Neuroscience.

[46]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. I. Method Descriptions and Simulations , 2004, Brain Topography.

[47]  P. Deltenre,et al.  Mismatch negativity evoked by the McGurk–MacDonald effect: a phonetic representation within short-term memory , 2002, Clinical Neurophysiology.

[48]  J. Decety,et al.  From the perception of action to the understanding of intention , 2001, Nature reviews. Neuroscience.

[49]  R. Hari,et al.  Suppressed responses to self-triggered sounds in the human auditory cortex. , 2004, Cerebral cortex.

[50]  Mikko Sams,et al.  Processing of changes in visual speech in the human auditory cortex. , 2002, Brain research. Cognitive brain research.

[51]  T. Takeda,et al.  Modulation of early auditory processing by visually based sound prediction , 2006, Brain Research.

[52]  C. C. Wood,et al.  Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. , 1985, Electroencephalography and clinical neurophysiology.

[53]  Alexandra Fort,et al.  Interest and validity of the additive model in electrophysiological studies of multisensory interactions , 2004, Cognitive Processing.

[54]  M. Giard,et al.  Auditory-Visual Integration during Multimodal Object Recognition in Humans: A Behavioral and Electrophysiological Study , 1999, Journal of Cognitive Neuroscience.

[55]  R Freedman,et al.  Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. , 1982, Biological psychiatry.

[56]  J. Vroomen,et al.  Perception of intersensory synchrony: A tutorial review , 2010, Attention, perception & psychophysics.

[57]  T. Picton,et al.  The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. , 1987, Psychophysiology.

[58]  Jean Vroomen,et al.  Neural Correlates of Multisensory Integration of Ecologically Valid Audiovisual Events , 2007, Journal of Cognitive Neuroscience.

[59]  Mikko Sams,et al.  Seeing speech affects acoustic information processing in the human brainstem , 2005, Experimental Brain Research.

[60]  J. Ford,et al.  Fine-tuning of auditory cortex during speech production. , 2005, Psychophysiology.

[61]  D. Barth,et al.  The spatiotemporal organization of auditory, visual, and auditory-visual evoked potentials in rat cortex , 1995, Brain Research.

[62]  Zhong-Lin Lu,et al.  Modification of sudden onset auditory ERP by involuntary attention to visual stimuli. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[63]  S A Hillyard,et al.  An analysis of audio-visual crossmodal integration by means of event-related potential (ERP) recordings. , 2002, Brain research. Cognitive brain research.

[64]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[65]  G. Meyer,et al.  Electrophysiological correlates of facial configuration and audio–visual congruency: evidence that face processing is a visual rather than a multisensory task , 2011, Experimental Brain Research.