Cortical processing of lateral skin stretch stimulation in humans

Direction discrimination of a moving tactile stimulus requires intact dorsal columns and provides a sensitive clinical test of somatosensory dysfunction. Cortical mechanisms are poorly understood. We have applied tangential skin pulls to the right lower leg during functional magnetic resonance imaging. Healthy subjects judged the direction of the skin pulls (task experiment, n = 7) or received skin pulls passively (no task experiment, n = 8). Second somatosensory cortex (S2) was activated in the task as well as no task experiment, and there was no significant difference in cortical activation between the two experiments. Within S2 nearly all subjects had prominent activations in the caudal and superficial part, i.e., in the opercular parietal (OP) area 1. S1 was activated in only one of the subjects. Thus, S2 and especially OP 1 seems to be important for processing of lateral skin stretch stimulation. The finding suggests that a lesion of this area might cause a disturbance in tactile direction discrimination which should be relevant for clinical testing.

[1]  U. Norrsell,et al.  Remarkable capacity for perception of the direction of skin pull in man , 1998, Brain Research.

[2]  A. Schleicher,et al.  The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. , 2006, Cerebral cortex.

[3]  U. Norrsell,et al.  Spatial cues serving the tactile directional sensibility of the human forearm. , 1994, The Journal of physiology.

[4]  J. Hyvärinen,et al.  I. Functional properties of neurons in lateral part of associative area 7 in awake monkeys , 1979, Experimental Brain Research.

[5]  K. Amunts,et al.  The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. , 2006, Cerebral cortex.

[6]  B. Edin Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. , 1992, Journal of neurophysiology.

[7]  F. McGlone,et al.  Unmyelinated tactile afferents underpin detection of low‐force monofilaments , 2006, Muscle & nerve.

[8]  Y. Lamarre,et al.  Unmyelinated tactile afferents signal touch and project to insular cortex , 2002, Nature Neuroscience.

[9]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

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

[11]  A. Benton,et al.  Tactile perception of direction in relation to handedness and familial handedness , 1975, Neuropsychologia.

[12]  J. Wessberg,et al.  Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin. , 1999, Journal of neurophysiology.

[13]  G H Duncan,et al.  Cortical activation by tactile and painful stimuli in hemispherectomized patients. , 2001, Brain : a journal of neurology.

[14]  E P Gardner,et al.  Simulation of motion on the skin. V. Effect of stimulus temporal frequency on the representation of moving bar patterns in primary somatosensory cortex of monkeys. , 1992, Journal of neurophysiology.

[15]  H. Sakata,et al.  Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. , 1973, Brain research.

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

[17]  G. Hankey,et al.  The utility of testing tactile perception of direction of scratch as a sensitive clinical sign of posterior column dysfunction in spinal cord disorders. , 1989, Journal of neurology, neurosurgery, and psychiatry.

[18]  J. Wessberg,et al.  Tactile directional sensibility: peripheral neural mechanisms in man , 2000, Brain Research.

[19]  O. Foerster Symptomatologie der Erkrankungen des Rückenmarks und seiner Wurzeln , 1936 .

[20]  Oswald Bumke,et al.  Handbuch der Neurologie , 1936 .

[21]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[22]  Patrick D. Wall,et al.  SENSORY FUNCTIONS WHICH REMAIN IN MAN AFTER COMPLETE TRANSECTION OF DORSAL COLUMNS , 1977 .

[23]  W. R. Gould,et al.  Cues Supporting Recognition of the Orientation or Direction of Movement of Tactile Stimuli , 1979 .

[24]  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.

[25]  E. P. Gardner,et al.  A quantitative analysis of responses of direction-sensitive neurons in somatosensory cortex of awake monkeys. , 1980, Journal of neurophysiology.

[26]  U. Norrsell Defects in Tactile Directional Sensitivity after Forebrain Commissurotomy in Man , 1973, Nature.

[27]  M. B. Bender,et al.  Agraphesthesia A disorder of directional cutaneous kinesthesia or a disorientation in cutaneous space , 1982, Journal of the Neurological Sciences.

[28]  R. Sekuler,et al.  Sensitive, objective procedure for evaluating response to light touch , 1973, Neurology.

[29]  R. Johansson,et al.  Encoding of Direction of Fingertip Forces by Human Tactile Afferents , 2001, The Journal of Neuroscience.

[30]  Karl J. Friston,et al.  Neural Coding of Tactile Decisions in the Human Prefrontal Cortex , 2006, The Journal of Neuroscience.

[31]  G. Werner,et al.  Cortical information processing of stimulus motion on primate skin. , 1972, Journal of neurophysiology.

[32]  Christian Maihöfner,et al.  Neural activation during experimental allodynia: a functional magnetic resonance imaging study , 2004, The European journal of neuroscience.

[33]  M. Paré,et al.  Magnitude estimation of tangential force applied to the fingerpad , 2002, Experimental Brain Research.

[34]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[35]  Mandayam A. Srinivasan,et al.  Tangential versus normal displacements of skin: relative effectiveness for producing tactile sensations , 2002, Proceedings 10th Symposium on Haptic Interfaces for Virtual Environment and Teleoperator Systems. HAPTICS 2002.

[36]  H Burton,et al.  Tactile attention tasks enhance activation in somatosensory regions of parietal cortex: a positron emission tomography study. , 1999, Cerebral cortex.

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

[38]  B L Whitsel,et al.  The response of SI directionally selective neurons to stimulus motion occurring at two sites within the receptive field. , 1993, Somatosensory & motor research.

[39]  Johan Wessberg,et al.  Discriminative touch and emotional touch. , 2007, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[40]  G. Essick,et al.  Tactile motion activates the human middle temporal/V5 (MT/V5) complex , 2002, The European journal of neuroscience.

[41]  A. Ptito,et al.  Tactile functions after cerebral hemispherectomy , 2005, Neuropsychologia.

[42]  Alan C. Evans,et al.  A general statistical analysis for fMRI data , 2000, NeuroImage.