Somatotopy and Attentional Modulation of the Human Parietal and Opercular Regions

The somatotopical organization of the postcentral gyrus is well known, but less is known about the somatotopical organization of area 2, the somatosensory association areas in the postparietal cortex, and the parietal operculum. The extent to which these areas are modulated by attention is also poorly understood. For these reasons, we measured the BOLD signal when rectangular parallelepipeds of varying shape were presented to the immobile right hand or right foot of 10 subjects either discriminating these or just being stimulated. Activation areas in each subject were mapped against cytoarchitectural probability maps of area 2, IP1, and IP2 along the intraparietal sulcus and the parietal opercular areas OP1-OP4. In area 2, the somatotopical representation of the hand and foot were distinctly separate, whereas there was considerable overlap in IP1 and no clear evidence of separate representations in OP1, OP4, and IP2. The overlap of hand and foot representations increased in the following order: area 3a, 3b, 1, 2, IP1, OP4, IP2, and OP1. There were significant foot representations but no hand representations in right (ipsilateral) areas 3a, 3b, and 1. Shape discrimination using the foot as opposed to stimulation enhanced the signal in OP4 bilaterally, whereas discrimination with the hand enhanced the signal bilaterally in area 2, IP1, and IP2. These results indicate that somatosensory areas in humans are arranged from strong somatotopy into no somatotopy in the following order: 3a, 3b, 1, 2, IP1, OP4, IP2, and OP1. Higher order areas such as IP1, IP2, and OP4 showed task-related attentional enhancement.

[1]  P. Roland,et al.  Comparison of spatial normalization procedures and their impact on functional maps , 2002, Human brain mapping.

[2]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[3]  Per E. Roland,et al.  Somatosensory detection of microgeometry, macrogeometry and kinesthesia in man , 1987, Brain Research Reviews.

[4]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[5]  Keiji Tanaka,et al.  Optical Imaging of Functional Organization in the Monkey Inferotemporal Cortex , 1996, Science.

[6]  L Krubitzer,et al.  A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Hiroshi Shibasaki,et al.  Second somatosensory area (SII) plays a significant role in selective somatosensory attention. , 2002, Brain research. Cognitive brain research.

[8]  K. Zilles,et al.  Illusory Arm Movements Activate Cortical Motor Areas: A Positron Emission Tomography Study , 1999, The Journal of Neuroscience.

[9]  R. J. Seitz,et al.  Vibratory stimulation increases and decreases the regional cerebral blood flow and oxidative metabolism: a positron emission tomography (PET) study , 1992, Acta neurologica Scandinavica.

[10]  J. Miller,et al.  Early prognosis after severe human head injury utilizing multimodality evoked potentials. , 1979, Acta neurochirurgica. Supplementum.

[11]  H Burton,et al.  Multiple foci in parietal and frontal cortex activated by rubbing embossed grating patterns across fingerpads: a positron emission tomography study in humans. , 1997, Cerebral cortex.

[12]  B Milner,et al.  Somatosensory thresholds--contrasting effects of postcentral-gyrus and posterior parietal-lobe excisions. , 1970, Archives of neurology.

[13]  W. Penfield The Cerebral Cortex of Man , 1950 .

[14]  Karl J. Friston,et al.  Multisubject fMRI Studies and Conjunction Analyses , 1999, NeuroImage.

[15]  G. Holmes,et al.  Sensory disturbances from cerebral lesions , 1911 .

[16]  P. Roland,et al.  Focal increase of cerebral blood flow during stereognostic testing in man. , 1976, Archives of neurology.

[17]  K. Zilles,et al.  Structural divisions and functional fields in the human cerebral cortex 1 Published on the World Wide Web on 20 February 1998. 1 , 1998, Brain Research Reviews.

[18]  M D Ginsberg,et al.  Human task‐specific somatosensory activation , 1987, Neurology.

[19]  J. Maunsell,et al.  The role of attention in visual processing. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[20]  P E Roland,et al.  Somatotopical tuning of postcentral gyrus during focal attention in man. A regional cerebral blood flow study. , 1981, Journal of neurophysiology.

[21]  M. Raichle,et al.  Mapping human somatosensory cortex with positron emission tomography. , 1987, Journal of neurosurgery.

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

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

[24]  K. Zilles,et al.  Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI , 2000, Neurology.

[25]  Christian Bohm,et al.  Somatosensory Discrimination of Shape: Tactile Exploration and Cerebral Activation , 1991, The European journal of neuroscience.

[26]  J. Pardo,et al.  PET studies of somatosensory processing of light touch , 2002, Behavioural Brain Research.

[27]  M Hämäläinen,et al.  Neuromagnetic responses from the second somatosensory cortex in man , 1983, Acta neurologica Scandinavica.

[28]  G. Werner,et al.  Symmetry and connectivity in the map of the body surface in somatosensory area II of primates. , 1969, Journal of neurophysiology.

[29]  C. Woolsey,et al.  Contralateral, ipsilateral, and bilateral representation of cutaneous receptors in somatic areas I and II of the cerebral cortex of pig, sheep, and other mammals. , 1946, Surgery.

[30]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[31]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.

[32]  H Burton,et al.  Functional MRI in human somatosensory cortex activated by touching textured surfaces , 1996, Journal of magnetic resonance imaging : JMRI.

[33]  David C. Alsop,et al.  Mapping of secondary somatosensory cortex activation induced by vibrational stimulation: an fMRI study , 1999, Brain Research.

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

[35]  Paolo Maria Rossini,et al.  Topographic Organization of the Human Primary and Secondary Somatosensory Cortices: Comparison of fMRI and MEG Findings , 2002, NeuroImage.

[36]  Maurizio Corbetta,et al.  Functional reorganization and stability of somatosensory-motor cortical topography in a tetraplegic subject with late recovery , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Per E. Roland,et al.  Some principles and new methods of tactile stimulation , 1975 .

[38]  P. Roland Organization of motor control by the normal human brain. , 1984, Human neurobiology.

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

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

[41]  Tore Risch,et al.  A database generator for human brain imaging , 2001, Trends in Neurosciences.

[42]  大石 健一 Cortical motor areas in plantar response : an event-related functional magnetic resonance imaging study in normal subjects , 2005 .

[43]  G. Chelune,et al.  Neurocognitive studies in patients with supplementary sensorimotor area lesions. , 1996, Advances in neurology.

[44]  S. Huckins,et al.  Patterns of lateral sensory cortical activation determined using functional magnetic resonance imaging. , 1998, Journal of neurosurgery.

[45]  P. Roland,et al.  Shape and roughness activate different somatosensory areas in the human brain. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[46]  David P. Friedman,et al.  Representation pattern in the second somatic sensory area of the monkey cerebral cortex , 1980, The Journal of comparative neurology.

[47]  P. Roland,et al.  I Feel My Hand Moving A New Role of the Primary Motor Cortex in Somatic Perception of Limb Movement , 2002, Neuron.

[48]  H Burton,et al.  Somatotopographic organization in the second somatosensory area of M. fascicularis , 1980, The Journal of comparative neurology.

[49]  U Salvolini,et al.  Localization of the first and second somatosensory areas in the human cerebral cortex with functional MR imaging. , 1999, AJNR. American journal of neuroradiology.

[50]  W.J.R. Dunseath,et al.  fMRI of the Responses to Vibratory Stimulation of Digit Tips , 2000, NeuroImage.

[51]  K. Zilles,et al.  Crossmodal Processing of Object Features in Human Anterior Intraparietal Cortex An fMRI Study Implies Equivalencies between Humans and Monkeys , 2002, Neuron.

[52]  Ryuta Kawashima,et al.  A PET Study of Somatosensory Discrimination in Man. Microgeometry Versus Macrogeometry , 1994, The European journal of neuroscience.

[53]  P. Morosan,et al.  Observer-Independent Method for Microstructural Parcellation of Cerebral Cortex: A Quantitative Approach to Cytoarchitectonics , 1999, NeuroImage.

[54]  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.

[55]  O. Bumke,et al.  Handbuch der Neurologie , 1936 .

[56]  R Kawashima,et al.  Changes in rCBF during grasping in humans examined by PET , 1996, Neuroreport.

[57]  K. Zilles,et al.  Fast reaction to different sensory modalities activates common fields in the motor areas, but the anterior cingulate cortex is involved in the speed of reaction. , 2000, Journal of neurophysiology.

[58]  P. Roland,et al.  Somatosensory Activations of the Parietal Operculum of Man. A PET Study , 1995, The European journal of neuroscience.

[59]  P E Roland,et al.  Somatosensory areas in man activated by moving stimuli: cytoarchitectonic mapping and PET , 2000, Neuroreport.

[60]  Mara Fabri,et al.  Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: A revised interpretation of the second somatosensory area in macaque monkeys , 1995, The Journal of comparative neurology.

[61]  A. Alavi,et al.  Positron emission tomographic studies of sensory stimuli, cognitive processes and anxiety. , 1983, Human neurobiology.

[62]  P Servos,et al.  fMRI-derived cortical maps for haptic shape, texture, and hardness. , 2001, Brain research. Cognitive brain research.

[63]  Simon B. Eickhoff,et al.  Cytoarchitectonic analysis and stereotaxic map of the human secondary somatosensory cortex region , 2002 .

[64]  K. Zilles,et al.  Hierarchical Processing of Tactile Shape in the Human Brain , 2001, Neuron.

[65]  M. Raichle,et al.  Tactile-vibration-activated foci in insular and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans. , 1993, Somatosensory & motor research.

[66]  J. Kaas,et al.  Multiple representations of the body within the primary somatosensory cortex of primates. , 1979, Science.

[67]  L. Krubitzer,et al.  Evidence for interhemispheric processing of inputs from the hands in human S2 and PV. , 2001, Journal of neurophysiology.

[68]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[69]  I. Kaufman The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1951 .