Tactile estimation of the roughness of gratings yields a graded response in the human brain: an fMRI study

Human subjects can tactually estimate the magnitude of surface roughness. Although many psychophysical and neurophysiological experiments have elucidated the peripheral neural mechanisms that underlie tactile roughness estimation, the associated cortical mechanisms are not well understood. To identify the brain regions responsible for the tactile estimation of surface roughness, we used functional magnetic resonance imaging (fMRI). We utilized a combination of categorical (subtraction) and parametric factorial approaches wherein roughness was varied during both the task and its control. Fourteen human subjects performed a tactile roughness-estimation task and received the identical tactile stimulation without estimation (no-estimation task). The bilateral parietal operculum (PO), insula and right lateral prefrontal cortex showed roughness-related activation. The bilateral PO and insula showed activation during the no-estimation task, and hence might represent the sensory-based processing during roughness estimation. By contrast, the right prefrontal cortex is more related to the cognitive processing, as there was activation during the estimation task compared with the no-estimation task, but little activation was observed during the no-estimation task in comparison with rest. The lateral prefrontal area might play an important cognitive role in tactile estimation of surface roughness, whereas the PO and insula might be involved in the sensory processing that is important for estimating surface roughness.

[1]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[2]  J. Baron Hindcasting nitrogen deposition to determine an ecological critical load. , 2006, Ecological applications : a publication of the Ecological Society of America.

[3]  Patricia S. Goldman TOPOGRAPHY OF COGNITION: Parallel Distributed Networks in Primate Association Cortex , 1988 .

[4]  Alan C. Evans,et al.  Distributed processing of pain and vibration by the human brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  M. Hollins,et al.  Vibrotactile adaptation impairs discrimination of fine, but not coarse, textures. , 2001, Somatosensory & motor research.

[6]  Roland Bobbink,et al.  Impacts of tropospheric ozone and airborne nitrogenous pollutants on natural and semi‐natural ecosystems: a commentary , 1998 .

[7]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[8]  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.

[9]  J. Ponsford Tactile spatial resolution in blind Braille readers , 2000, Neurology.

[10]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[11]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  Kenneth O. Johnson,et al.  Review: Neural Coding and the Basic Law of Psychophysics , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[13]  W. McIlroy,et al.  Task‐relevant selective modulation of somatosensory afferent paths from the lower limb , 2000, Neuroreport.

[14]  Á. Pascual-Leone,et al.  Tactile spatial resolution in blind Braille readers , 2000, Neurology.

[15]  H Burton,et al.  Attending to and Remembering Tactile Stimuli: A Review of Brain Imaging Data and Single-Neuron Responses , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[16]  G. T. Coleman,et al.  Functional characteristics of the parallel SI- and SII-projecting neurons of the thalamic ventral posterior nucleus in the marmoset. , 2001, Journal of neurophysiology.

[17]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[18]  Hiroshi Shibasaki,et al.  Attention modulates both primary and second somatosensory cortical activities in humans: a magnetoencephalographic study. , 1998, Journal of neurophysiology.

[19]  M. Loreau,et al.  Biodiversity as spatial insurance in heterogeneous landscapes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Rüdiger J. Seitz,et al.  A fronto-parietal circuit for tactile object discrimination: an event-related fMRI study , 2003, NeuroImage.

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

[23]  J. Greenspan,et al.  Reversible pain and tactile deficits associated with a cerebral tumor compressing the posterior insula and parietal operculum , 1992, Pain.

[24]  Ingrid M. Kanics,et al.  Tactile Acuity is Enhanced in Blindness , 2003, The Journal of Neuroscience.

[25]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[26]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

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

[28]  Sandra E. Black,et al.  Task-Relevant Modulation of Contralateral and Ipsilateral Primary Somatosensory Cortex and the Role of a Prefrontal-Cortical Sensory Gating System , 2002, NeuroImage.

[29]  J. Peterson,et al.  Imperiled Waters, Impoverished Future: The Decline of Freshwater Ecosystems , 1996 .

[30]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[31]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[32]  David P. Friedman,et al.  Thalamic connectivity of the second somatosensory area and neighboring somatosensory fields of the lateral sulcus of the macaque , 1986, The Journal of comparative neurology.

[33]  Karl J. Friston,et al.  1 A taxonomy of study design , 1997 .

[34]  Emilio Salinas,et al.  Cognitive neuroscience: Flutter Discrimination: neural codes, perception, memory and decision making , 2003, Nature Reviews Neuroscience.

[35]  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.

[36]  K. O. Johnson,et al.  Roughness coding in the somatosensory system. , 1993, Acta psychologica.

[37]  L A Krubitzer,et al.  The organization and connections of somatosensory cortex in marmosets , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  J. Hunter Downs,et al.  FMRI mapping of the somatosensory cortex with vibratory stimuli Is there a dependency on stimulus frequency? , 2001, Brain Research.

[39]  M. Hollins,et al.  Vibrotaction and texture perception , 2002, Behavioural Brain Research.

[40]  Kenneth O. Johnson,et al.  Neural Coding Mechanisms Underlying Perceived Roughness of Finely Textured Surfaces , 2001, The Journal of Neuroscience.

[41]  原田 宗子,et al.  Asymmetrical neural substrates of tactile discrimination in humans : a functional magnetic resonance imaging study , 2005 .

[42]  K L Woodward,et al.  The relationship between skin compliance, age, gender, and tactile discriminative thresholds in humans. , 1993, Somatosensory & motor research.

[43]  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.

[44]  P. Goldman-Rakic,et al.  Connections of the ventral granular frontal cortex of macaques with perisylvian premotor and somatosensory areas: Anatomical evidence for somatic representation in primate frontal association cortex , 1989, The Journal of comparative neurology.

[45]  G. T. Coleman,et al.  Hierarchical equivalence of somatosensory areas I and II for tactile processing in the cerebral cortex of the marmoset monkey. , 2001, Journal of neurophysiology.

[46]  Simon J Graham,et al.  Activation in SI and SII: the influence of vibrotactile amplitude during passive and task-relevant stimulation. , 2004, Brain research. Cognitive brain research.

[47]  M Corbetta,et al.  Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Alan K. Knapp,et al.  Photosynthetic and Water Relations Responses to Elevated CO2 in the C4 Grass Andropogon gerardii , 1993, International Journal of Plant Sciences.

[49]  Jill S. Baron,et al.  Anthropogenic nitrogen deposition induces rapid ecological changes in alpine lakes of the Colorado Front Range (USA) , 2001 .

[50]  Á. Pascual-Leone,et al.  Tactile spatial resolution in blind Braille readers , 2000, Neurology.

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

[52]  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.

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

[54]  H Hämäläinen,et al.  Activation of somatosensory cortical areas varies with attentional state: an fMRI study , 2002, Behavioural Brain Research.

[55]  J. Keeley,et al.  Role of high fire frequency in destruction of mixed chaparral. , 1993 .

[56]  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.

[57]  Van Boven RW,et al.  Tactile spatial resolution in blind braille readers(1) , 2000, American journal of ophthalmology.

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