Functional MRI indicates consistent intra-digit topographic maps in the little but not the index finger within the human primary somatosensory cortex

This study explored the question of intra-digit somatotopy of sensory representations in the little and index finger of 10 subjects using tactile stimulation of the fingertip (p1) and base (p4) and functional magnetic resonance imaging (fMRI) at 1.5mm isotropic spatial resolution. The Euclidian distances between p1 and p4 peak representations in Brodmann area 3b resulted in 5.0±0.7mm for the little finger and 6.7±0.5mm for the index finger. These non-collocated representations were found to be consistently ordered across subjects for the little but not the index finger. When using separate distances for medial-lateral, anterior-posterior, and inferior-superior orientations, p4 was 1.9±0.7mm medial to p1 for the little finger in agreement with findings in macaque monkeys, whereas no consistent intra-digit somatotopy across subjects was found for the index finger. This discrepancy could point to differences in the map-forming processes based on sensory input. On the behavioral level it may be attributed to our everyday use of the hand, for which p4 of the index finger plays a much less important role than p4 of the little finger, which is located at the outer border of the hand.

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

[2]  I. Hashimoto,et al.  Distal-proximal somatotopy in the human hand somatosensory cortex: a reappraisal , 1999, Experimental Brain Research.

[3]  A Villringer,et al.  fMRI assessment of somatotopy in human Brodmann area 3b by electrical finger stimulation , 1998, Neuroreport.

[4]  F. McGlone,et al.  The cutaneous sensory system , 2010, Neuroscience & Biobehavioral Reviews.

[5]  O. Hikosaka,et al.  Converging patterns of finger representation and complex response properties of neurons in area 1 of the first somatosensory cortex of the conscious monkey , 1983, Experimental Brain Research.

[6]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[7]  Jelliffe.  Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

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

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

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

[11]  M. Merzenich,et al.  Representation of slowly and rapidly adapting cutaneous mechanoreceptors of the hand in Brodmann's areas 3 and 1 of Macaca mulatta. , 1972, Brain research.

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

[13]  Philip Servos,et al.  Distributed digit somatotopy in primary somatosensory cortex , 2004, NeuroImage.

[14]  J. Kaas,et al.  Double representation of the body surface within cytoarchitectonic area 3b and 1 in “SI” in the owl monkey (aotus trivirgatus) , 1978, The Journal of comparative neurology.

[15]  Isao Hashimoto,et al.  Serial N20m dipoles in somatosensory evoked magnetic fields move along the distal-proximal representation of the digit area 3b of the human cortex , 2004, Neuroscience Letters.

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

[17]  V. Mountcastle,et al.  The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. , 1968, Journal of neurophysiology.

[18]  O. Arthurs,et al.  What aspect of the fMRI BOLD signal best reflects the underlying electrophysiology in human somatosensory cortex? , 2003, Clinical Neurophysiology.

[19]  David C. Alsop,et al.  The Sensory Somatotopic Map of the Human Hand Demonstrated at 4 Tesla , 1999, NeuroImage.

[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]  Jan Ruben,et al.  Evidence for a rostral-to-caudal somatotopic organization in human primary somatosensory cortex with mirror-reversal in areas 3b and 1. , 2003, Cerebral cortex.

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

[23]  Riitta Hari,et al.  Distal-to-proximal representation of volar index finger in human area 3b , 2004, NeuroImage.

[24]  R. Johansson,et al.  Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. , 1979, The Journal of physiology.

[25]  V. Mountcastle,et al.  Detection thresholds for stimuli in humans and monkeys: comparison with threshold events in mechanoreceptive afferent nerve fibers innervating the monkey hand. , 1972, Journal of neurophysiology.

[26]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

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

[28]  Toshiaki Imada,et al.  Are there discrete distal-proximal representations of the index finger and palm in the human somatosensory cortex? A neuromagnetic study , 1999, Clinical Neurophysiology.

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

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

[31]  M. Sur,et al.  Representations of the body surface in postcentral parietal cortex of Macaca fascicularis , 1980, The Journal of comparative neurology.

[32]  O. Hikosaka,et al.  Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey , 1983, Experimental Brain Research.

[33]  J. Kaas,et al.  Variability in hand surface representations in areas 3b and 1 in adult owl and squirrel monkeys , 1987, The Journal of comparative neurology.

[34]  V. Mountcastle,et al.  Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. , 1959, Bulletin of the Johns Hopkins Hospital.