Four-dimensional maps of the human somatosensory system

Significance Here, we show how anatomical and functional data recorded from patients undergoing stereo-EEG can be combined to generate highly resolved four-dimensional maps of human cortical processing. We used this technique, which provides spatial maps of the active cortical nodes at a millisecond scale, to depict the somatosensory processing following electrical stimulation of the median nerve in nearly 100 patients. The results showed that human somatosensory system encompasses a widespread cortical network including a phasic component, centered on primary somatosensory cortex and neighboring motor, premotor, and inferior parietal regions, as well as a tonic component, centered on the opercular and insular areas, lasting more than 200 ms. A fine-grained description of the spatiotemporal dynamics of human brain activity is a major goal of neuroscientific research. Limitations in spatial and temporal resolution of available noninvasive recording and imaging techniques have hindered so far the acquisition of precise, comprehensive four-dimensional maps of human neural activity. The present study combines anatomical and functional data from intracerebral recordings of nearly 100 patients, to generate highly resolved four-dimensional maps of human cortical processing of nonpainful somatosensory stimuli. These maps indicate that the human somatosensory system devoted to the hand encompasses a widespread network covering more than 10% of the cortical surface of both hemispheres. This network includes phasic components, centered on primary somatosensory cortex and neighboring motor, premotor, and inferior parietal regions, and tonic components, centered on opercular and insular areas, and involving human parietal rostroventral area and ventral medial-superior-temporal area. The technique described opens new avenues for investigating the neural basis of all levels of cortical processing in humans.

[1]  Philippe Kahane,et al.  Direct Evidence for Two Different Neural Mechanisms for Reading Familiar and Unfamiliar Words: An Intra-Cerebral EEG Study , 2011, Front. Hum. Neurosci..

[2]  Rafael Malach,et al.  Intracranial recordings reveal transient response dynamics during information maintenance in human cerebral cortex , 2015, Human brain mapping.

[3]  Gereon R Fink,et al.  The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. , 2007, Cerebral cortex.

[4]  K. Amunts,et al.  The human inferior parietal lobule in stereotaxic space , 2008, Brain Structure and Function.

[5]  P. Pietrini,et al.  Mind the blind brain to understand the sighted one! Is there a supramodal cortical functional architecture? , 2014, Neuroscience & Biobehavioral Reviews.

[6]  Lauri Parkkonen,et al.  The brain timewise: how timing shapes and supports brain function , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  Leah Krubitzer,et al.  Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys , 2003, The Journal of comparative neurology.

[8]  M. Kahana,et al.  Synchronous and Asynchronous Theta and Gamma Activity during Episodic Memory Formation , 2013, The Journal of Neuroscience.

[9]  F. Cardinale,et al.  Stereo‐electroencephalography safety and effectiveness: Some more reasons in favor of epilepsy surgery , 2013, Epilepsia.

[10]  M. Frot,et al.  Early secondary somatosensory area (SII) SEPs. Data from intracerebral recordings in humans , 2002, Clinical Neurophysiology.

[11]  Timothy Edward John Behrens,et al.  Diffusion-Weighted Imaging Tractography-Based Parcellation of the Human Lateral Premotor Cortex Identifies Dorsal and Ventral Subregions with Anatomical and Functional Specializations , 2007, The Journal of Neuroscience.

[12]  A Villringer,et al.  Somatotopic organization of human secondary somatosensory cortex. , 2001, Cerebral cortex.

[13]  Francesco Sala,et al.  Steady-state activation in somatosensory cortex after changes in stimulus rate during median nerve stimulation. , 2009, Magnetic resonance imaging.

[14]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[15]  A. Iggo,et al.  Somatosensory System , 1973 .

[16]  R. Hari,et al.  Functional Organization of the Human First and Second Somatosensory Cortices: a Neuromagnetic Study , 1993, The European journal of neuroscience.

[17]  L. Krubitzer,et al.  Somatotopic organization of cortical fields in the lateral sulcus of Homo sapiens: Evidence for SII and PV , 2000, The Journal of comparative neurology.

[18]  Roland Peyron,et al.  Spatial segregation of somato-sensory and pain activations in the human operculo-insular cortex , 2012, NeuroImage.

[19]  C. Munari,et al.  Stereo‐electroencephalography methodology: advantages and limits , 1994, Acta neurologica Scandinavica. Supplementum.

[20]  G. Orban,et al.  The Retinotopic Organization of the Human Middle Temporal Area MT/V5 and Its Cortical Neighbors , 2010, The Journal of Neuroscience.

[21]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[22]  Philippe Kahane,et al.  Efficient “Pop-Out” Visual Search Elicits Sustained Broadband Gamma Activity in the Dorsal Attention Network , 2012, The Journal of Neuroscience.

[23]  Juha Virtanen,et al.  Activation of multiple cortical areas in response to somatosensory stimulation: Combined magnetoencephalographic and functional magnetic resonance imaging , 1999, Human brain mapping.

[24]  Francesco Cardinale,et al.  Stereoelectroencephalography in the Presurgical Evaluation of Focal Epilepsy: A Retrospective Analysis of 215 Procedures , 2005, Neurosurgery.

[25]  K. Zilles,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 2. Spatial Normalization to Standard Anatomical Space , 2000, NeuroImage.

[26]  E. Halgren,et al.  High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research , 2012, Progress in Neurobiology.

[27]  A. Turman,et al.  PARALLEL ORGANIZATION OF SOMATOSENSORY CORTICAL AREAS I AND II FOR TACTILE PROCESSING , 1996, Clinical and experimental pharmacology & physiology.

[28]  Nitin Tandon,et al.  Surface-based mixed effects multilevel analysis of grouped human electrocorticography , 2014, NeuroImage.

[29]  Philippe Kahane,et al.  Probabilistic functional tractography of the human cortex , 2013, NeuroImage.

[30]  P. Avanzini,et al.  Sequencing Biological and Physical Events Affects Specific Frequency Bands within the Human Premotor Cortex: An Intracerebral EEG Study , 2014, PloS one.

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

[32]  Pierre Rainville,et al.  Serial processing in primary and secondary somatosensory cortex: A DCM analysis of human fMRI data in response to innocuous and noxious electrical stimulation , 2014, Neuroscience Letters.

[33]  P. Rousseeuw Silhouettes: a graphical aid to the interpretation and validation of cluster analysis , 1987 .

[34]  M. Kramer,et al.  Beyond the Connectome: The Dynome , 2014, Neuron.

[35]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[36]  Rafael Malach,et al.  Spatial and Object-Based Attention Modulates Broadband High-Frequency Responses across the Human Visual Cortical Hierarchy , 2013, The Journal of Neuroscience.

[37]  Arno Villringer,et al.  Dynamic causal modeling suggests serial processing of tactile vibratory stimuli in the human somatosensory cortex—An fMRI study , 2013, NeuroImage.

[38]  C J Hodge,et al.  Functional magnetic resonance imaging of somatosensory cortex activity produced by electrical stimulation of the median nerve or tactile stimulation of the index finger. , 2000, Journal of neurosurgery.

[39]  P. Morosan,et al.  Broca's Region: Novel Organizational Principles and Multiple Receptor Mapping , 2010, PLoS biology.

[40]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[41]  Sergio Tufik,et al.  Afferent pain pathways: a neuroanatomical review , 2004, Brain Research.

[42]  Joseph R. Madsen,et al.  Individualized localization and cortical surface-based registration of intracranial electrodes , 2012, NeuroImage.

[43]  T. Powell,et al.  Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions. , 1969, Brain : a journal of neurology.

[44]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[45]  J. Sarvas,et al.  Mixed and sensory nerve stimulations activate different cytoarchitectonic areas in the human primary somatosensory cortex SI , 1986, Experimental Brain Research.

[46]  J. Kaas CHAPTER 28 – Somatosensory System , 2004 .

[47]  Nitin Tandon,et al.  Category specific spatial dissociations of parallel processes underlying visual naming. , 2014, Cerebral cortex.

[48]  Nitin Tandon,et al.  Development of grouped icEEG for the study of cognitive processing , 2015, Front. Psychol..

[49]  A. Mouraux,et al.  Parallel Processing of Nociceptive and Non-nociceptive Somatosensory Information in the Human Primary and Secondary Somatosensory Cortices: Evidence from Dynamic Causal Modeling of Functional Magnetic Resonance Imaging Data , 2011, The Journal of Neuroscience.

[50]  A. Schleicher,et al.  Cytoarchitectonic analysis of the human extrastriate cortex in the region of V5/MT+: a probabilistic, stereotaxic map of area hOc5. , 2006, Cerebral cortex.

[51]  A. Engel,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.12 Single-trial EEG–fMRI reveals the dynamics of cognitive function , 2022 .

[52]  R. Hari,et al.  Modified activation of somatosensory cortical network in patients with right-hemisphere stroke. , 1999, Brain : a journal of neurology.

[53]  P. Avanzini,et al.  Human cortical activity evoked by gaze shift observation: An intracranial EEG study , 2014, Human brain mapping.

[54]  R. Hari,et al.  Phase locking between human primary and secondary somatosensory cortices , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[55]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. , 1988, Journal of neurophysiology.

[56]  C. Grimm,et al.  A new method to measure cortical growth in the developing brain. , 2010, Journal of biomechanical engineering.

[57]  G. Orban,et al.  Coding observed motor acts: different organizational principles in the parietal and premotor cortex of humans. , 2010, Journal of neurophysiology.

[58]  Mark Jenkinson,et al.  Correspondences between retinotopic areas and myelin maps in human visual cortex , 2014, NeuroImage.

[59]  Juan R. Vidal,et al.  Category-Specific Visual Responses: An Intracranial Study Comparing Gamma, Beta, Alpha, and ERP Response Selectivity , 2010, Front. Hum. Neurosci..

[60]  Michael S. Beauchamp,et al.  Re-examining overlap between tactile and visual motion responses within hMT+ and STS , 2015, NeuroImage.

[61]  D. V. van Essen,et al.  Structural and Functional Analyses of Human Cerebral Cortex Using a Surface-Based Atlas , 1997, The Journal of Neuroscience.

[62]  J. Karhu,et al.  Simultaneous early processing of sensory input in human primary (SI) and secondary (SII) somatosensory cortices. , 1999, Journal of neurophysiology.

[63]  Rajesh P. N. Rao,et al.  Real-time functional brain mapping using electrocorticography , 2007, NeuroImage.

[64]  R Salmelin,et al.  Comparison of somatosensory evoked fields to airpuff and electric stimuli. , 1994, Electroencephalography and clinical neurophysiology.

[65]  Christian Wallraven,et al.  Intra- and inter-hemispheric effective connectivity in the human somatosensory cortex during pressure stimulation , 2014, BMC Neuroscience.

[66]  Felix Blankenburg,et al.  Tactile and visual motion direction processing in hMT+/V5 , 2014, NeuroImage.

[67]  Leah Krubitzer,et al.  The organization and connections of anterior and posterior parietal cortex in titi monkeys: do New World monkeys have an area 2? , 2005, Cerebral cortex.

[68]  Katrin Amunts,et al.  The human inferior parietal cortex: Cytoarchitectonic parcellation and interindividual variability , 2006, NeuroImage.

[69]  Matt Stead,et al.  Human Neuroscience , 2022 .

[70]  Milan Sonka,et al.  3D Slicer as an image computing platform for the Quantitative Imaging Network. , 2012, Magnetic resonance imaging.

[71]  B. Burle,et al.  Spatial and temporal resolutions of EEG: Is it really black and white? A scalp current density view , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[72]  D. V. Essen,et al.  Cartography and Connectomes , 2013, Neuron.

[73]  T. Powell,et al.  Connexions of the somatic sensory cortex of the rhesus monkey. I. Ipsilateral cortical connexions. , 1969, Brain : a journal of neurology.

[74]  C. Babiloni,et al.  Somatotopy of anterior cingulate cortex (ACC) and supplementary motor area (SMA) for electric stimulation of the median and tibial nerves: An fMRI study , 2006, NeuroImage.

[75]  David C. Van Essen,et al.  Cortical cartography and Caret software , 2012, NeuroImage.

[76]  Claudio Babiloni,et al.  Cortical brain responses during passive nonpainful median nerve stimulation at low frequencies (0.5–4 Hz): An fMRI study , 2007, Human brain mapping.

[77]  Katrin Amunts,et al.  Architecture and organizational principles of Broca's region , 2012, Trends in Cognitive Sciences.

[78]  Srikantan S Nagarajan,et al.  Sensorimotor integration in S2, PV, and parietal rostroventral areas of the human sylvian fissure. , 2007, Journal of neurophysiology.

[79]  Nikolaus M. Szeverenyi,et al.  Fingertip Representation in the Human Somatosensory Cortex: An fMRI Study , 1998, NeuroImage.

[80]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[81]  U. Ilg,et al.  Primate area MST-l is involved in the generation of goal-directed eye and hand movements. , 2007, Journal of neurophysiology.