Distinct fine‐scale fMRI activation patterns of contra‐ and ipsilateral somatosensory areas 3b and 1 in humans

Inter‐areal and ipsilateral cortical responses to tactile stimulation have not been well described in human S1 cortex. By taking advantage of the high signal‐to‐noise ratio at 7 T, we quantified blood oxygenation level dependent (BOLD) response patterns and time courses to tactile stimuli on individual distal finger pads at a fine spatial scale, and examined whether there are inter‐areal (area 3b versus area 1) and interhemispheric response differences to unilateral tactile stimulation in healthy human subjects. We found that 2‐Hz tactile stimulation of individual fingertips evoked detectable BOLD signal changes in both contralateral and ipsilateral area 3b and area 1. Contralateral digit activations were organized in an orderly somatotopic manner, and BOLD responses in area 3b were more digit selective than those in area 1. However, the area of cortex that was responsive to stimulation of a single digit (stimulus–response field) was similar across areas. In the ipsilateral hemisphere, response magnitudes in both areas 3b and 1 were significantly weaker than those of the contralateral hemisphere. Digit activations exhibited no clear somatotopic organizational pattern in either area 3b or area 1, yet digit selectivity was retained in area 1 but not in area 3b. The observation of distinct digit‐selective responses of contralateral area 3b versus area 1 supports a higher order function of contralateral area 1 in spatial integration. In contrast, ipsilateral cortices may play a less discriminative role in the perception of unilateral tactile sensation in humans. Hum Brain Mapp 35:4841–4857, 2014. © 2014 Wiley Periodicals, Inc.

[1]  Richard Bowtell,et al.  Regional structural differences across functionally parcellated Brodmann areas of human primary somatosensory cortex , 2014, NeuroImage.

[2]  Olaf Blanke,et al.  Human finger somatotopy in areas 3b, 1, and 2: A 7T fMRI study using a natural stimulus , 2014, Human brain mapping.

[3]  G. Kranz,et al.  High-resolution functional MRI of the human amygdala at 7 T , 2013, European journal of radiology.

[4]  Denis Schluppeck,et al.  Single-subject fMRI mapping at 7 T of the representation of fingertips in S1: a comparison of event-related and phase-encoding designs. , 2013, Journal of neurophysiology.

[5]  Karsten Mueller,et al.  The functional architecture of S1 during touch observation described with 7 T fMRI , 2013, Brain Structure and Function.

[6]  Noam Harel Ultra high resolution fMRI at ultra-high field , 2012, NeuroImage.

[7]  Jeff H. Duyn,et al.  The future of ultra-high field MRI and fMRI for study of the human brain , 2012, NeuroImage.

[8]  M. Wibral,et al.  Spatiotemporal Dynamics of Bimanual Integration in Human Somatosensory Cortex and Their Relevance to Bimanual Object Manipulation , 2012, The Journal of Neuroscience.

[9]  Frank Tong,et al.  Multishot versus Single-Shot Pulse Sequences in Very High Field fMRI: A Comparison Using Retinotopic Mapping , 2012, PloS one.

[10]  Rishma Vidyasagar,et al.  Reproducibility of functional MRI localization within the human somatosensory cortex , 2011, Journal of magnetic resonance imaging : JMRI.

[11]  Jens Frahm,et al.  Functional MRI indicates consistent intra-digit topographic maps in the little but not the index finger within the human primary somatosensory cortex , 2011, NeuroImage.

[12]  Jamie L. Reed,et al.  Spatiotemporal Properties of Neuron Response Suppression in Owl Monkey Primary Somatosensory Cortex When Stimuli Are Presented to Both Hands , 2011, The Journal of Neuroscience.

[13]  John C. Gore,et al.  Differentiation of somatosensory cortices by high-resolution fMRI at 7T , 2011, NeuroImage.

[14]  C. Schroeder,et al.  Interactions within the Hand Representation in Primary Somatosensory Cortex of Primates , 2010, The Journal of Neuroscience.

[15]  Essa Yacoub,et al.  Retinotopic mapping with spin echo BOLD at 7T. , 2010, Magnetic resonance imaging.

[16]  Lawrence L. Wald,et al.  Laminar analysis of 7T BOLD using an imposed spatial activation pattern in human V1 , 2010, NeuroImage.

[17]  A. Keller,et al.  Abnormal activity of primary somatosensory cortex in central pain syndrome. , 2010, Journal of neurophysiology.

[18]  Katrin Amunts,et al.  Cytoarchitecture and probabilistic maps of the human posterior insular cortex. , 2010, Cerebral cortex.

[19]  John C. Gore,et al.  Challenges and Opportunities of Ultra-High Field MRI , 2010 .

[20]  S. Francis,et al.  Mapping human somatosensory cortex in individual subjects with 7 T functional MRI 1 Running title : Mapping human somatosensory cortex , 2010 .

[21]  S. C. Gandevia,et al.  Neuropathic pain and primary somatosensory cortex reorganization following spinal cord injury , 2009, PAIN®.

[22]  K Zilles,et al.  Functional lateralization of face, hand, and trunk representation in anatomically defined human somatosensory areas. , 2008, Cerebral cortex.

[23]  Anna W Roe,et al.  Responses of areas 3b and 1 in anesthetized squirrel monkeys to single- and dual-site stimulation of the digits. , 2008, Journal of neurophysiology.

[24]  Robert Chen,et al.  Digit somatotopy within cortical areas of the postcentral gyrus in humans. , 2008, Cerebral cortex.

[25]  J. Baizabal-Carvallo,et al.  A case of tactile agnosia with a lesion restricted to the post-central gyrus. , 2008, Neurology India.

[26]  Jens Frahm,et al.  Finger representations in human primary somatosensory cortex as revealed by high-resolution functional MRI of tactile stimulation , 2008, NeuroImage.

[27]  John C Gore,et al.  High-Resolution Maps of Real and Illusory Tactile Activation in Primary Somatosensory Cortex in Individual Monkeys with Functional Magnetic Resonance Imaging and Optical Imaging , 2007, The Journal of Neuroscience.

[28]  Patrick Ragert,et al.  Improvement of tactile perception and enhancement of cortical excitability through intermittent theta burst rTMS over human primary somatosensory cortex , 2007, Experimental Brain Research.

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

[30]  Essa Yacoub,et al.  Spatio-temporal point-spread function of fMRI signal in human gray matter at 7 Tesla , 2007, NeuroImage.

[31]  Srikantan S Nagarajan,et al.  Spatiotemporal integration of tactile information in human somatosensory cortex , 2007, BMC Neuroscience.

[32]  H. Flor,et al.  Phantom limb pain: a case of maladaptive CNS plasticity? , 2006, Nature Reviews Neuroscience.

[33]  Essa Yacoub,et al.  Frontiers of brain mapping using MRI , 2006, Journal of magnetic resonance imaging : JMRI.

[34]  Mark Tommerdahl,et al.  Ipsilateral Input Modifies the Primary Somatosensory Cortex Response to Contralateral Skin Flutter , 2006, The Journal of Neuroscience.

[35]  Riitta Hari,et al.  Transient Suppression of Ipsilateral Primary Somatosensory Cortex during Tactile Finger Stimulation , 2006, The Journal of Neuroscience.

[36]  Michael L. Lipton,et al.  Ipsilateral Hand Input to Area 3b Revealed by Converging Hemodynamic and Electrophysiological Analyses in Macaque Monkeys , 2006, The Journal of Neuroscience.

[37]  Li Min Chen,et al.  Optical Imaging of SI Topography in Anesthetized and Awake Squirrel Monkeys , 2005, The Journal of Neuroscience.

[38]  Takeo Ishigaki,et al.  Contralateral and ipsilateral responses in primary somatosensory cortex following electrical median nerve stimulation—an fMRI study , 2005, Clinical Neurophysiology.

[39]  Hubert Preissl,et al.  The right hand knows what the left hand is feeling , 2005, Experimental Brain Research.

[40]  C. Porro,et al.  Percept-related activity in the human somatosensory system: functional magnetic resonance imaging studies. , 2004, Magnetic resonance imaging.

[41]  C. Xerri,et al.  Deficits and recovery of body stabilization during acrobatic locomotion after focal lesion to the somatosensory cortex: a kinematic analysis combined with cortical mapping. , 2004, Archives italiennes de biologie.

[42]  Masahiro Sakamoto,et al.  Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus , 2004, Experimental Brain Research.

[43]  F. Esposito,et al.  High field functional MRI. , 2003, European journal of radiology.

[44]  A. Sbarbati,et al.  High field MRI in preclinical research. , 2003, European journal of radiology.

[45]  Anna W. Roe,et al.  Optical Imaging of a Tactile Illusion in Area 3b of the Primary Somatosensory Cortex , 2003, Science.

[46]  H. Dinse,et al.  Functional Imaging of Perceptual Learning in Human Primary and Secondary Somatosensory Cortex , 2003, Neuron.

[47]  Hirobumi Oikawa,et al.  High-field MRI of the central nervous system: current approaches to clinical and microscopic imaging. , 2003, Magnetic resonance in medical sciences : MRMS : an official journal of Japan Society of Magnetic Resonance in Medicine.

[48]  A. A Ioannides,et al.  The human primary somatosensory cortex response contains components related to stimulus frequency and perception in a frequency discrimination task , 2003, Neuroscience.

[49]  H. Flor Cortical reorganisation and chronic pain: implications for rehabilitation. , 2003, Journal of rehabilitation medicine.

[50]  K. Uğurbil,et al.  Spin‐echo fMRI in humans using high spatial resolutions and high magnetic fields , 2003, Magnetic resonance in medicine.

[51]  Jon H Kaas,et al.  The organization of somatosensory cortex in anthropoid primates. , 2003, Advances in neurology.

[52]  J. Kaas,et al.  Anatomic and functional reorganization of somatosensory cortex in mature primates after peripheral nerve and spinal cord injury. , 2003, Advances in neurology.

[53]  S. Bohlhalter,et al.  Hierarchical versus parallel processing in tactile object recognition: a behavioural-neuroanatomical study of aperceptive tactile agnosia. , 2002, Brain : a journal of neurology.

[54]  Christoph Stippich,et al.  Interaction of Tactile Input in the Human Primary and Secondary Somatosensory Cortex—A Magnetoencephalographic Study , 2001, NeuroImage.

[55]  K. Zilles,et al.  Human Somatosensory Area 2: Observer-Independent Cytoarchitectonic Mapping, Interindividual Variability, and Population Map , 2001, NeuroImage.

[56]  R. Romo,et al.  Tactile Shape Processing , 2001, Neuron.

[57]  Gabriel Curio,et al.  Representational overlap of adjacent fingers in multiple areas of human primary somatosensory cortex depends on electrical stimulus intensity: an fMRI study , 2001, Brain Research.

[58]  Justin A. Harris,et al.  The Topography of Tactile Learning in Humans , 2001, The Journal of Neuroscience.

[59]  A M Dale,et al.  Segregation of somatosensory activation in the human rolandic cortex using fMRI. , 2000, Journal of neurophysiology.

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

[61]  Y X Wang,et al.  Leu‐enkephalin induced by IL‐2 administration mediates analgesic effect of IL‐2 , 2000, Neuroreport.

[62]  A Villringer,et al.  fMRI shows multiple somatotopic digit representations in human primary somatosensory cortex , 2000, Neuroreport.

[63]  K. Zilles,et al.  t Object Shape Differences Reflected by Somatosensory Cortical Activation , 2000, The Journal of Neuroscience.

[64]  M. Bushnell,et al.  Pain perception: is there a role for primary somatosensory cortex? , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[65]  A. Schleicher,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 1. Microstructural Organization and Interindividual Variability , 1999, NeuroImage.

[66]  Y. Iwamura Hierarchical somatosensory processing , 1998, Current Opinion in Neurobiology.

[67]  Emilio Salinas,et al.  Role of primary somatic sensory cortex in the categorization of tactile stimuli: effects of lesions , 1997, Experimental Brain Research.

[68]  S Noachtar,et al.  Ipsilateral median somatosensory evoked potentials recorded from human somatosensory cortex. , 1997, Electroencephalography and clinical neurophysiology.

[69]  Niels Birbaumer,et al.  Extensive reorganization of primary somatosensory cortex in chronic back pain patients , 1997, Neuroscience Letters.

[70]  L. White,et al.  Structure of the human sensorimotor system. I: Morphology and cytoarchitecture of the central sulcus. , 1997, Cerebral cortex.

[71]  Riitta Salmelin,et al.  Tactile information from the human hand reaches the ipsilateral primary somatosensory cortex , 1995, Neuroscience Letters.

[72]  P. Jezzard,et al.  Correction for geometric distortion in echo planar images from B0 field variations , 1995, Magnetic resonance in medicine.

[73]  H Burton,et al.  Ipsilateral intracortical connections of physiologically defined cutaneous representations in areas 3b and 1 of macaque monkeys: Projections in the vicinity of the central sulcus , 1995, The Journal of comparative neurology.

[74]  P. Mckinley,et al.  Age-dependent differences in reorganization of primary somatosensory cortex following low thoracic (T12) spinal cord transection in cats , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[76]  R. Klatzky,et al.  Hand movements: A window into haptic object recognition , 1987, Cognitive Psychology.

[77]  J. Kaas,et al.  Consistent features of the representation of the hand in area 3b of macaque monkeys. , 1987, Somatosensory research.

[78]  M. Fabri,et al.  Bilateral receptive fields and callosal connectivity of the body midline representation in the first somatosensory area of primates. , 1986, Somatosensory research.

[79]  J. H. Kaas,et al.  A sequential representation of the occiput, arm, forearm and hand across the rostrocaudal dimension of areas 1, 2 and 5 in macaque monkeys , 1985, Brain Research.

[80]  J. Kaas,et al.  The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys , 1983, The Journal of comparative neurology.

[81]  J. Kaas,et al.  Representations of the body surface in cortical areas 3b and 1 of squirrel monkeys: Comparisons with other primates , 1982, The Journal of comparative neurology.

[82]  J. Kaas,et al.  Magnification, receptive-field area, and "hypercolumn" size in areas 3b and 1 of somatosensory cortex in owl monkeys. , 1980, Journal of neurophysiology.

[83]  R H LaMotte,et al.  Disorders in somesthesis following lesions of parietal lobe. , 1979, Journal of neurophysiology.