Onset timing of cross‐sensory activations and multisensory interactions in auditory and visual sensory cortices

Here we report early cross‐sensory activations and audiovisual interactions at the visual and auditory cortices using magnetoencephalography (MEG) to obtain accurate timing information. Data from an identical fMRI experiment were employed to support MEG source localization results. Simple auditory and visual stimuli (300‐ms noise bursts and checkerboards) were presented to seven healthy humans. MEG source analysis suggested generators in the auditory and visual sensory cortices for both within‐modality and cross‐sensory activations. fMRI cross‐sensory activations were strong in the visual but almost absent in the auditory cortex; this discrepancy with MEG possibly reflects the influence of acoustical scanner noise in fMRI. In the primary auditory cortices (Heschl’s gyrus) the onset of activity to auditory stimuli was observed at 23 ms in both hemispheres, and to visual stimuli at 82 ms in the left and at 75 ms in the right hemisphere. In the primary visual cortex (Calcarine fissure) the activations to visual stimuli started at 43 ms and to auditory stimuli at 53 ms. Cross‐sensory activations thus started later than sensory‐specific activations, by 55 ms in the auditory cortex and by 10 ms in the visual cortex, suggesting that the origins of the cross‐sensory activations may be in the primary sensory cortices of the opposite modality, with conduction delays (from one sensory cortex to another) of 30–35 ms. Audiovisual interactions started at 85 ms in the left auditory, 80 ms in the right auditory and 74 ms in the visual cortex, i.e., 3–21 ms after inputs from the two modalities converged.

[1]  Abbreviations , 1971 .

[2]  G. Celesia Organization of auditory cortical areas in man. , 1976, Brain : a journal of neurology.

[3]  L. Benevento,et al.  Auditory-visual interaction in single cells in the cortex of the superior temporal sulcus and the orbital frontal cortex of the macaque monkey , 1977, Experimental Neurology.

[4]  R Desimone,et al.  Both striate cortex and superior colliculus contribute to visual properties of neurons in superior temporal polysensory area of macaque monkey. , 1986, Journal of neurophysiology.

[5]  M. Hämäläinen,et al.  Realistic conductivity geometry model of the human head for interpretation of neuromagnetic data , 1989, IEEE Transactions on Biomedical Engineering.

[6]  C. Gross Contribution of striate cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and inferior temporal cortex , 1991, Neuropsychologia.

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

[8]  K. Rockland,et al.  Direct temporal-occipital feedback connections to striate cortex (V1) in the macaque monkey. , 1994, Cerebral cortex.

[9]  C. Cusick,et al.  The Superior Temporal Polysensory Region in Monkeys , 1997 .

[10]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[11]  P. Bandettini,et al.  Functional MRI of brain activation induced by scanner acoustic noise , 1998, Magnetic resonance in medicine.

[12]  A K Liu,et al.  Spatiotemporal imaging of human brain activity using functional MRI constrained magnetoencephalography data: Monte Carlo simulations. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

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

[15]  R W Cox,et al.  Real‐time 3D image registration for functional MRI , 1999, Magnetic resonance in medicine.

[16]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[17]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[18]  A M Dale,et al.  Estimation and detection of event‐related fMRI signals with temporally correlated noise: A statistically efficient and unbiased approach , 2000, Human brain mapping.

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

[20]  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.

[21]  S. Inati,et al.  Eye Position Influences Auditory Responses in Primate Inferior Colliculus , 2001, Neuron.

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

[23]  G. V. Simpson,et al.  Flow of activation from V1 to frontal cortex in humans , 2001, Experimental Brain Research.

[24]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[25]  Barry E. Stein,et al.  Book Review: Cortex Governs Multisensory Integration in the Midbrain , 2002 .

[26]  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.

[27]  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.

[28]  Terrence R Stanford,et al.  Cortex governs multisensory integration in the midbrain. , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[29]  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.

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

[31]  J. Mazziotta,et al.  Brain Mapping: The Methods , 2002 .

[32]  G. R. Barnes,et al.  A Quantitative Assessment of the Sensitivity of Whole-Head MEG to Activity in the Adult Human Cortex , 2002, NeuroImage.

[33]  Anders M. Dale,et al.  Improved Localization of Cortical Activity By Combining EEG and MEG with MRI Cortical Surface Reconstruction , 2002 .

[34]  Seppo P. Ahlfors,et al.  New Six-Layer Magnetically-Shielded Room for MEG , 2002 .

[35]  R. Hari,et al.  10 – Magnetoencephalographic Characterization of Dynamic Brain Activation: Basic Principles and Methods of Data Collection and Source Analysis , 2002 .

[36]  Y. Yen,et al.  Deactivation of Sensory-Specific Cortex by Cross-Modal Stimuli , 2002, Journal of Cognitive Neuroscience.

[37]  S. Shimojo,et al.  Visual illusion induced by sound. , 2002, Brain research. Cognitive brain research.

[38]  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.

[39]  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.

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

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

[42]  Henry Kennedy,et al.  Long-distance feedback projections to area V1: Implications for multisensory integration, spatial awareness, and visual consciousness , 2004, Cognitive, affective & behavioral neuroscience.

[43]  Nikos Makris,et al.  Automatically parcellating the human cerebral cortex. , 2004, Cerebral cortex.

[44]  David C Lyon,et al.  Distribution across cortical areas of neurons projecting to the superior colliculus in new world monkeys. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[45]  Christoph M. Michel,et al.  Visuo-motor pathways in humans revealed by event-related fMRI , 2006, Experimental Brain Research.

[46]  John J. Foxe,et al.  The case for feedforward multisensory convergence during early cortical processing , 2005, Neuroreport.

[47]  John J. Foxe,et al.  Look 'hear', primary auditory cortex is active during lip-reading. , 2005, Neuroreport.

[48]  John J. Foxe,et al.  Multisensory contributions to low-level, ‘unisensory’ processing , 2005, Current Opinion in Neurobiology.

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

[50]  John J. Foxe,et al.  Grabbing your ear: rapid auditory-somatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment. , 2005, Cerebral cortex.

[51]  E. Macaluso,et al.  Multisensory spatial interactions: a window onto functional integration in the human brain , 2005, Trends in Neurosciences.

[52]  P. Barone,et al.  Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey , 2005, The European journal of neuroscience.

[53]  Lee M. Miller,et al.  Behavioral/systems/cognitive Perceptual Fusion and Stimulus Coincidence in the Cross- Modal Integration of Speech , 2022 .

[54]  Ladan Shams,et al.  Early modulation of visual cortex by sound: an MEG study , 2005, Neuroscience Letters.

[55]  M. Sams,et al.  Primary auditory cortex activation by visual speech: an fMRI study at 3 T , 2005, Neuroreport.

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

[57]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Geraint Rees,et al.  Sound alters activity in human V1 in association with illusory visual perception , 2006, NeuroImage.

[59]  E. Macaluso Multisensory Processing in Sensory-Specific Cortical Areas , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[60]  H. Scheich,et al.  Multisensory processing via early cortical stages: Connections of the primary auditory cortical field with other sensory systems , 2006, Neuroscience.

[61]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[62]  Lisa A. de la Mothe,et al.  Thalamic connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[63]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

[64]  Yoshinao Kajikawa,et al.  Cortical connections of the auditory cortex in marmoset monkeys: Core and medial belt regions , 2006, The Journal of comparative neurology.

[65]  A. Ghazanfar,et al.  Is neocortex essentially multisensory? , 2006, Trends in Cognitive Sciences.

[66]  M. Woldorff,et al.  Selective attention and audiovisual integration: is attending to both modalities a prerequisite for early integration? , 2006, Cerebral cortex.

[67]  Jean-Philippe Thiran,et al.  Multisensory interactions within human primary cortices revealed by BOLD dynamics. , 2007, Cerebral cortex.

[68]  Istvan Ulbert,et al.  Multisensory convergence in auditory cortex, II. Thalamocortical connections of the caudal superior temporal plane , 2007, The Journal of comparative neurology.

[69]  T. Hackett,et al.  Multisensory convergence in auditory cortex, I. Cortical connections of the caudal superior temporal plane in macaque monkeys , 2007, The Journal of comparative neurology.

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

[71]  A. Ioannides,et al.  Attention Modulates Earliest Responses in the Primary Auditory and Visual Cortices , 2008, Neuron.

[72]  Bruce R. Rosen,et al.  Parallel input makes the brain run faster , 2008, NeuroImage.

[73]  S. Celebrini,et al.  Visuo-auditory interactions in the primary visual cortex of the behaving monkey: Electrophysiological evidence , 2008, BMC Neuroscience.

[74]  O. Bertrand,et al.  Visual Activation and Audiovisual Interactions in the Auditory Cortex during Speech Perception: Intracranial Recordings in Humans , 2008, The Journal of Neuroscience.

[75]  Arnaud Falchier,et al.  Multisensory connections of monkey auditory cerebral cortex , 2009, Hearing Research.

[76]  V Solo,et al.  Dynamic Granger-Geweke causality modeling with application to interictal spike propagation , 2009, NeuroImage.

[77]  Céline Cappe,et al.  The Thalamocortical Projection Systems in Primate: An Anatomical Support for Multisensory and Sensorimotor Interplay , 2009, Cerebral cortex.

[78]  J. Schoffelen,et al.  Source connectivity analysis with MEG and EEG , 2009, Human brain mapping.

[79]  J. Mäkelä,et al.  Sources of auditory brainstem responses revisited: Contribution by magnetoencephalography , 2009, Human brain mapping.

[80]  C. Schroeder,et al.  Neuronal mechanisms, response dynamics and perceptual functions of multisensory interactions in auditory cortex , 2009, Hearing Research.

[81]  L. Vaina,et al.  Mapping the signal‐to‐noise‐ratios of cortical sources in magnetoencephalography and electroencephalography , 2009, Human brain mapping.

[82]  Micah M. Murray,et al.  Early, Low-Level Auditory-Somatosensory Multisensory Interactions Impact Reaction Time Speed , 2009, Front. Integr. Neurosci..

[83]  Robert T. Knight,et al.  Intermodal Auditory, Visual, and Tactile Attention Modulates Early Stages of Neural Processing , 2009, Journal of Cognitive Neuroscience.