Similarity-Based Fusion of MEG and fMRI Reveals Spatio-Temporal Dynamics in Human Cortex During Visual Object Recognition

Every human cognitive function, such as visual object recognition, is realized in a complex spatio-temporal activity pattern in the brain. Current brain imaging techniques in isolation cannot resolve the brain's spatio-temporal dynamics, because they provide either high spatial or temporal resolution but not both. To overcome this limitation, we developed an integration approach that uses representational similarities to combine measurements of magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) to yield a spatially and temporally integrated characterization of neuronal activation. Applying this approach to 2 independent MEG–fMRI data sets, we observed that neural activity first emerged in the occipital pole at 50–80 ms, before spreading rapidly and progressively in the anterior direction along the ventral and dorsal visual streams. Further region-of-interest analyses established that dorsal and ventral regions showed MEG–fMRI correspondence in representations later than early visual cortex. Together, these results provide a novel and comprehensive, spatio-temporally resolved view of the rapid neural dynamics during the first few hundred milliseconds of object vision. They further demonstrate the feasibility of spatially unbiased representational similarity-based fusion of MEG and fMRI, promising new insights into how the brain computes complex cognitive functions.

[1]  S. Taulu,et al.  Suppression of Interference and Artifacts by the Signal Space Separation Method , 2003, Brain Topography.

[2]  G. Yovel,et al.  Stimulation of Category-Selective Brain Areas Modulates ERP to Their Preferred Categories , 2011, Current Biology.

[3]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[4]  G. Rees,et al.  Predicting the Stream of Consciousness from Activity in Human Visual Cortex , 2005, Current Biology.

[5]  Michael S. Pratte,et al.  Decoding patterns of human brain activity. , 2012, Annual review of psychology.

[6]  Radoslaw Martin Cichy,et al.  Probing principles of large‐scale object representation: Category preference and location encoding , 2013, Human brain mapping.

[7]  Thomas A. Carlson,et al.  Emerging Object Representations in the Visual System Predict Reaction Times for Categorization , 2015, PLoS Comput. Biol..

[8]  Kenneth Hugdahl,et al.  Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potentials and functional MRI. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[9]  H. Sakata,et al.  Selectivity of the parietal visual neurones in 3D orientation of surface of stereoscopic stimuli. , 1996, Neuroreport.

[10]  K. Grill-Spector,et al.  The functional architecture of the ventral temporal cortex and its role in categorization , 2014, Nature Reviews Neuroscience.

[11]  Moritz Grosse-Wentrup,et al.  Multisubject Learning for Common Spatial Patterns in Motor-Imagery BCI , 2011, Comput. Intell. Neurosci..

[12]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[13]  Bruno Rossion,et al.  Parametric design and correlational analyses help integrating fMRI and electrophysiological data during face processing , 2004, NeuroImage.

[14]  Richard M. Leahy,et al.  A comparison of random field theory and permutation methods for the statistical analysis of MEG data , 2005, NeuroImage.

[15]  Nikos K. Logothetis,et al.  Three-Dimensional Shape Representation in Monkey Cortex , 2002, Neuron.

[16]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[17]  N. Kanwisher,et al.  How Distributed Is Visual Category Information in Human Occipito-Temporal Cortex? An fMRI Study , 2002, Neuron.

[18]  Maria C Romero,et al.  Responses to two‐dimensional shapes in the macaque anterior intraparietal area , 2012, The European journal of neuroscience.

[19]  R. Passingham,et al.  Reading Hidden Intentions in the Human Brain , 2007, Current Biology.

[20]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[21]  S. Kastner,et al.  Two hierarchically organized neural systems for object information in human visual cortex , 2008, Nature Neuroscience.

[22]  Radoslaw Martin Cichy,et al.  Resolving human object recognition in space and time , 2014, Nature Neuroscience.

[23]  Vince D. Calhoun,et al.  A review of multivariate methods for multimodal fusion of brain imaging data , 2012, Journal of Neuroscience Methods.

[24]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[25]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[26]  G. Mangun,et al.  Covariations in ERP and PET measures of spatial selective attention in human extrastriate visual cortex , 1997, Human brain mapping.

[27]  N. Kanwisher,et al.  Interpreting fMRI data: maps, modules and dimensions , 2008, Nature Reviews Neuroscience.

[28]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[29]  G. Kreiman,et al.  Timing, Timing, Timing: Fast Decoding of Object Information from Intracranial Field Potentials in Human Visual Cortex , 2009, Neuron.

[30]  R. M. Siegel,et al.  Neurons of area 7 activated by both visual stimuli and oculomotor behavior , 2004, Experimental Brain Research.

[31]  C. Koch,et al.  Latency and Selectivity of Single Neurons Indicate Hierarchical Processing in the Human Medial Temporal Lobe , 2008, The Journal of Neuroscience.

[32]  N. Kriegeskorte,et al.  Author ' s personal copy Representational geometry : integrating cognition , computation , and the brain , 2013 .

[33]  Karl J. Friston,et al.  EEG-fMRI integration: a critical review of biophysical modeling and data analysis approaches. , 2010, Journal of integrative neuroscience.

[34]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Liang Wang,et al.  Probabilistic Maps of Visual Topography in Human Cortex. , 2015, Cerebral cortex.

[36]  Radoslaw Martin Cichy,et al.  Imagery and perception share cortical representations of content and location. , 2012, Cerebral Cortex.

[37]  K. Grill-Spector,et al.  The human visual cortex. , 2004, Annual review of neuroscience.

[38]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[39]  Nikolaus Kriegeskorte,et al.  Un co rre cte d Pr oo f RT for Object Categorization Is Predicted by Representational Distance , 2013 .

[40]  Rainer Goebel,et al.  Tight covariation of BOLD signal changes and slow ERPs in the parietal cortex in a parametric spatial imagery task with haptic acquisition , 2006, The European journal of neuroscience.

[41]  J. Devlin,et al.  Triple Dissociation of Faces, Bodies, and Objects in Extrastriate Cortex , 2009, Current Biology.

[42]  Leila Reddy,et al.  Coding of visual objects in the ventral stream , 2006, Current Opinion in Neurobiology.

[43]  Alexander Borst,et al.  How does Nature Program Neuron Types? , 2008, Front. Neurosci..

[44]  Gabriel Kreiman,et al.  Visual population codes : toward a common multivariate framework for cell recording and functional imaging , 2012 .

[45]  Yi Chen,et al.  Encoding the identity and location of objects in human LOC , 2011, NeuroImage.

[46]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[47]  S. Taulu,et al.  Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements , 2006, Physics in medicine and biology.

[48]  A. Oliva,et al.  A Real-World Size Organization of Object Responses in Occipitotemporal Cortex , 2012, Neuron.

[49]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[50]  L. Tyler,et al.  Predicting the Time Course of Individual Objects with MEG , 2014, Cerebral cortex.

[51]  M. Goodale,et al.  Two visual systems re-viewed , 2008, Neuropsychologia.

[52]  E. Halgren,et al.  Spatiotemporal mapping of brain activity by integration of multiple imaging modalities , 2001, Current Opinion in Neurobiology.

[53]  David A. Tovar,et al.  Representational dynamics of object vision: the first 1000 ms. , 2013, Journal of vision.

[54]  Masaaki Kawahashi,et al.  Renovation of Journal of Visualization , 2010, J. Vis..

[55]  C. Connor,et al.  Population coding of shape in area V4 , 2002, Nature Neuroscience.

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

[57]  Keiji Tanaka,et al.  Object category structure in response patterns of neuronal population in monkey inferior temporal cortex. , 2007, Journal of neurophysiology.

[58]  Guy A. Orban,et al.  Visual Activation in Prefrontal Cortex is Stronger in Monkeys than in Humans , 2004, Journal of Cognitive Neuroscience.

[59]  Max C. Keuken,et al.  TMS over M1 Reveals Expression and Selective Suppression of Conflicting Action Impulses , 2014, Journal of Cognitive Neuroscience.

[60]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[61]  N. Kanwisher,et al.  Only some spatial patterns of fMRI response are read out in task performance , 2007, Nature Neuroscience.

[62]  John H. R. Maunsell,et al.  Shape selectivity in primate lateral intraparietal cortex , 1998, Nature.

[63]  A. Engel,et al.  Single-trial EEG–fMRI reveals the dynamics of cognitive function , 2006, Trends in Cognitive Sciences.

[64]  João Jorge,et al.  EEG–fMRI integration for the study of human brain function , 2014, NeuroImage.

[65]  N. Kanwisher,et al.  Multivariate Patterns in Object-Selective Cortex Dissociate Perceptual and Physical Shape Similarity , 2008, PLoS biology.

[66]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[67]  The Brain in Health and Disease – from Molecules to Man , 2001, Brain Research Reviews.

[68]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[69]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[70]  Joel Z. Leibo,et al.  The dynamics of invariant object recognition in the human visual system. , 2014, Journal of neurophysiology.

[71]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[72]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[73]  Michael D. Rugg,et al.  Latencies of visually responsive neurons in various regions of the rhesus monkey brain and their relation to human visual responses , 1988, Biological Psychology.

[74]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[75]  G. Orban,et al.  Coding of Shape and Position in Macaque Lateral Intraparietal Area , 2008, The Journal of Neuroscience.

[76]  J. Haynes Brain Reading: Decoding Mental States From Brain Activity In Humans , 2011 .

[77]  S. R. Lehky,et al.  Comparison of shape encoding in primate dorsal and ventral visual pathways. , 2007, Journal of neurophysiology.

[78]  David J. Freedman,et al.  Dynamic population coding of category information in inferior temporal and prefrontal cortex. , 2008, Journal of neurophysiology.

[79]  René J. Huster,et al.  Methods for Simultaneous EEG-fMRI: An Introductory Review , 2012, The Journal of Neuroscience.