Grabbing your ear: rapid auditory-somatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment.

Multisensory interactions are observed in species from single-cell organisms to humans. Important early work was primarily carried out in the cat superior colliculus and a set of critical parameters for their occurrence were defined. Primary among these were temporal synchrony and spatial alignment of bisensory inputs. Here, we assessed whether spatial alignment was also a critical parameter for the temporally earliest multisensory interactions that are observed in lower-level sensory cortices of the human. While multisensory interactions in humans have been shown behaviorally for spatially disparate stimuli (e.g. the ventriloquist effect), it is not clear if such effects are due to early sensory level integration or later perceptual level processing. In the present study, we used psychophysical and electrophysiological indices to show that auditory-somatosensory interactions in humans occur via the same early sensory mechanism both when stimuli are in and out of spatial register. Subjects more rapidly detected multisensory than unisensory events. At just 50 ms post-stimulus, neural responses to the multisensory 'whole' were greater than the summed responses from the constituent unisensory 'parts'. For all spatial configurations, this effect followed from a modulation of the strength of brain responses, rather than the activation of regions specifically responsive to multisensory pairs. Using the local auto-regressive average source estimation, we localized the initial auditory-somatosensory interactions to auditory association areas contralateral to the side of somatosensory stimulation. Thus, multisensory interactions can occur across wide peripersonal spatial separations remarkably early in sensory processing and in cortical regions traditionally considered unisensory.

[1]  John J. Foxe,et al.  Human–simian correspondence in the early cortical processing of multisensory cues , 2004, Cognitive Processing.

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

[3]  Christoph M. Michel,et al.  Electrical neuroimaging based on biophysical constraints , 2004, NeuroImage.

[4]  Christoph M. Michel,et al.  Rapid discrimination of visual and multisensory memories revealed by electrical neuroimaging , 2004, NeuroImage.

[5]  John J. Foxe,et al.  Multisensory Convergence in Early Cortical Processing. , 2004 .

[6]  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.

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

[8]  J. Hyvärinen,et al.  Functional properties of neurons in the temporo-parietal association cortex of awake monkey , 2004, Experimental Brain Research.

[9]  T. Hackett,et al.  Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[10]  M. L. Demattè,et al.  Beyond the window: multisensory representation of peripersonal space across a transparent barrier. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[11]  Kathleen S Rockland,et al.  Multisensory convergence in calcarine visual areas in macaque monkey. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[12]  Wan Jiang,et al.  Cortex controls multisensory depression in superior colliculus. , 2003, Journal of neurophysiology.

[13]  Riitta Hari,et al.  Activation of the human posterior parietal and temporoparietal cortices during audiotactile interaction , 2003, NeuroImage.

[14]  Ankoor S. Shah,et al.  Auditory Cortical Neurons Respond to Somatosensory Stimulation , 2003, The Journal of Neuroscience.

[15]  C. Spence,et al.  Multisensory integration and the body schema: close to hand and within reach , 2003, Current Biology.

[16]  Tirin Moore,et al.  Complex movements evoked by microstimulation of the ventral intraparietal area , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  L. Erasmus,et al.  Multisensory integration after traumatic brain injury: a reaction time study between pairings of vision, touch and audition , 2003, Brain injury.

[18]  Douglas S Brungart,et al.  Auditory localization in the horizontal plane with single and double hearing protection. , 2002, Aviation, space, and environmental medicine.

[19]  Lawrence E Marks,et al.  Cross-modal enhancement of perceived brightness: Sensory interaction versus response bias , 2003, Perception & psychophysics.

[20]  M. Wallace,et al.  Visual Localization Ability Influences Cross-Modal Bias , 2003, Journal of Cognitive Neuroscience.

[21]  N. Bolognini,et al.  Enhancement of visual perception by crossmodal visuo-auditory interaction , 2002, Experimental Brain Research.

[22]  Jean-Philippe Thiran,et al.  What and Where in human audition: selective deficits following focal hemispheric lesions , 2002, Experimental Brain Research.

[23]  John J. Foxe,et al.  Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. , 2002, Journal of neurophysiology.

[24]  H. Kennedy,et al.  Anatomical Evidence of Multimodal Integration in Primate Striate Cortex , 2002, The Journal of Neuroscience.

[25]  John J. Foxe,et al.  The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. , 2002, Brain research. Cognitive brain research.

[26]  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.

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

[28]  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.

[29]  J Driver,et al.  Crossmodal Spatial Influences of Touch on Extrastriate Visual Areas Take Current Gaze Direction into Account , 2002, Neuron.

[30]  Juliana Yordanova,et al.  Spatial coincidence modulates interaction between visual and somatosensory evoked potentials , 2002, Neuroreport.

[31]  C. Spence,et al.  Tactile “capture” of audition , 2002, Perception & psychophysics.

[32]  Christoph M. Michel,et al.  Segregated Processing of Auditory Motion and Auditory Location: An ERP Mapping Study , 2002, NeuroImage.

[33]  C. Lammertmann,et al.  Magnetoencephalographic Correlates of Audiotactile Interaction , 2002, NeuroImage.

[34]  Cristiana Cavina-Pratesi,et al.  Redundant target effect and intersensory facilitation from visual-tactile interactions in simple reaction time , 2002, Experimental Brain Research.

[35]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[36]  E. Ldavas,et al.  Auditory Peripersonal Space in Humans , 2002, Journal of Cognitive Neuroscience.

[37]  F. Rösler,et al.  Crossmodal and intermodal attention modulate event-related brain potentials to tactile and auditory stimuli , 2002, Experimental Brain Research.

[38]  John J. Foxe,et al.  Visuo-spatial neural response interactions in early cortical processing during a simple reaction time task: a high-density electrical mapping study , 2001, Neuropsychologia.

[39]  G. Calvert Crossmodal processing in the human brain: insights from functional neuroimaging studies. , 2001, Cerebral cortex.

[40]  H. Onoe,et al.  Functional Brain Mapping of Monkey Tool Use , 2001, NeuroImage.

[41]  S. Morand,et al.  Electric source imaging of human brain functions , 2001, Brain Research Reviews.

[42]  C. Schroeder,et al.  Somatosensory input to auditory association cortex in the macaque monkey. , 2001, Journal of neurophysiology.

[43]  E. J. Tehovnik,et al.  Eye Movements Modulate Visual Receptive Fields of V4 Neurons , 2001, Neuron.

[44]  G. Recanzone,et al.  Temporal and spatial dependency of the ventriloquism effect , 2001, Neuroreport.

[45]  S. Shimojo,et al.  Illusions: What you see is what you hear , 2000, Nature.

[46]  F. Wörgötter,et al.  Context, state and the receptive fields of striatal cortex cells , 2000, Trends in Neurosciences.

[47]  John J. Foxe,et al.  Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. , 2000, Brain research. Cognitive brain research.

[48]  C. Spence,et al.  Visual Capture of Touch: Out-of-the-Body Experiences With Rubber Gloves , 2000, Psychological science.

[49]  C. Tesche,et al.  Evidence for somatosensory evoked responses in human temporal lobe , 2000, Neuroreport.

[50]  C. Frith,et al.  Modulation of human visual cortex by crossmodal spatial attention. , 2000, Science.

[51]  C. Spence,et al.  Attracting attention to the illusory location of a sound: reflexive crossmodal orienting and ventriloquism , 2000, Neuroreport.

[52]  G H Recanzone,et al.  Correlation between the activity of single auditory cortical neurons and sound-localization behavior in the macaque monkey. , 2000, Journal of neurophysiology.

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

[54]  Dominic W. Massaro,et al.  Speechreading: illusion or window into pattern recognition , 1999, Trends in Cognitive Sciences.

[55]  J. Kaas,et al.  Auditory processing in primate cerebral cortex , 1999, Current Opinion in Neurobiology.

[56]  J. Fell,et al.  Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography , 1999, Human brain mapping.

[57]  E. Schröger,et al.  Speeded responses to audiovisual signal changes result from bimodal integration. , 1998, Psychophysiology.

[58]  C. K. Peck,et al.  Spatial disparity affects visual-auditory interactions in human sensorimotor processing , 1998, Experimental Brain Research.

[59]  Guldin Wo,et al.  Is there a vestibular cortex , 1998 .

[60]  O. Grüsser,et al.  Is there a vestibular cortex? , 1998, Trends in Neurosciences.

[61]  V. Jousmäki,et al.  Parchment-skin illusion: sound-biased touch , 1998, Current Biology.

[62]  S. Clarke,et al.  Cytochrome Oxidase, Acetylcholinesterase, and NADPH-Diaphorase Staining in Human Supratemporal and Insular Cortex: Evidence for Multiple Auditory Areas , 1997, NeuroImage.

[63]  R. Sekuler,et al.  Sound alters visual motion perception , 1997, Nature.

[64]  B. Stein,et al.  Enhancement of Perceived Visual Intensity by Auditory Stimuli: A Psychophysical Analysis , 1996, Journal of Cognitive Neuroscience.

[65]  Volker Hömberg,et al.  Sound localization in egocentric space following hemispheric lesions , 1996, Neuropsychologia.

[66]  M T Wallace,et al.  Comparisons of cross-modality integration in midbrain and cortex. , 1996, Progress in brain research.

[67]  D. Lehmann,et al.  Segmentation of brain electrical activity into microstates: model estimation and validation , 1995, IEEE Transactions on Biomedical Engineering.

[68]  A. Kimura,et al.  Effects of visual and auditory stimuli on median nerve somatosensory evoked potentials in man. , 1995, Electromyography and clinical neurophysiology.

[69]  P. Reuter-Lorenz,et al.  Visual-auditory interactions in sensorimotor processing: saccades versus manual responses. , 1994, Journal of experimental psychology. Human perception and performance.

[70]  Joseph E. LeDoux,et al.  Somatosensory and auditory convergence in the lateral nucleus of the amygdala. , 1993, Behavioral neuroscience.

[71]  M. Ahissar,et al.  Encoding of sound-source location and movement: activity of single neurons and interactions between adjacent neurons in the monkey auditory cortex. , 1992, Journal of neurophysiology.

[72]  David L. Sparks,et al.  Sensori-motor integration in the primate superior colliculus , 1991 .

[73]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[74]  Lawrence G. McDade,et al.  Behavioral Indices of Multisensory Integration: Orientation to Visual Cues is Affected by Auditory Stimuli , 1989, Journal of Cognitive Neuroscience.

[75]  B. Stein,et al.  Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  Antoine Rémond,et al.  Methods of Analysis of Brain Electrical and Magnetic Signals , 1987 .

[77]  D. Lehmann,et al.  Principles of spatial analysis , 1987 .

[78]  F. Perrin,et al.  Mapping of scalp potentials by surface spline interpolation. , 1987, Electroencephalography and clinical neurophysiology.

[79]  D L Sparks,et al.  Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals. , 1987, Journal of neurophysiology.

[80]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[81]  Jeff Miller,et al.  Divided attention: Evidence for coactivation with redundant signals , 1982, Cognitive Psychology.

[82]  D. H. Warren,et al.  The role of visual-auditory “compellingness” in the ventriloquism effect: Implications for transitivity among the spatial senses , 1981, Perception & psychophysics.

[83]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[84]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[85]  T. Powell,et al.  An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. , 1970, Brain : a journal of neurology.

[86]  D. Raab DIVISION OF PSYCHOLOGY: STATISTICAL FACILITATION OF SIMPLE REACTION TIMES* , 1962 .

[87]  D. Raab Statistical facilitation of simple reaction times. , 1962, Transactions of the New York Academy of Sciences.

[88]  W. H. Sumby,et al.  Visual contribution to speech intelligibility in noise , 1954 .

[89]  G. J. Thomas Experimental study of the influence of vision on sound localization. , 1941 .