Differential effects of cognitive demand on human cortical activation associated with vibrotactile stimulation.

This event-related functional MRI study examines the neural correlates of vibrotactile sensation within the context of different psychophysical demands. Nine subjects received vibrotactile stimuli on the right volar forearm during detection, localization, and passive tasks. In the detection task, subjects indicated the offset (end) of each stimulus by pressing a response key with their left hand. In the localization task, subjects identified the location of the stimulus ("distal?" or "proximal?") by pressing the appropriate response key 4 s after the end of the stimulus. In the passive task, subjects received the same vibrotactile stimuli, but no response was required. Analysis of stimulus-evoked activity compared with the resting baseline period revealed significant bilateral secondary somatosensory cortex activation for all three tasks. However, only in the offset-detection and localization tasks was stimulus-evoked activation observed in other expected areas of tactile processing, such as contralateral primary somatosensory cortex neighboring the posterior parietal cortex (SI/PPC) and in bilateral anterior insular cortex (aIC). During the localization task, we identified vibrotactile-evoked activation in the right aIC, which was maintained after the termination of the stimulus. Results suggest that vibrotactile-related activation within SI/PPC and aIC is enhanced by the increased levels of attention and cognitive demands required by the detection and localization tasks. Activation of aIC not only during vibrotactile stimulation, but also during the poststimulus delay in the localization trials, is consistent with the growing literature linking this area with the perception and short-term memory of tactile information.

[1]  M. Carreras,et al.  Functional properties of neurons of the anterior ectosylvian gyrus of the cat. , 1963, Journal of neurophysiology.

[2]  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.

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

[4]  Michael J. Martinez,et al.  The Role of the Insular Cortex in Pitch Pattern Perception: The Effect of Linguistic Contexts , 2004, The Journal of Neuroscience.

[5]  R. Treede,et al.  Human brain mechanisms of pain perception and regulation in health and disease , 2005, European journal of pain.

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

[7]  D. Linden,et al.  The Working Memory Networks of the Human Brain , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[8]  Felix M. Mottaghy,et al.  Human brain structures related to plantar vibrotactile stimulation: A functional magnetic resonance imaging study , 2006, NeuroImage.

[9]  C. L. Kwan,et al.  Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli. , 1998, Journal of neurophysiology.

[10]  Bernd J. Krause,et al.  Variability of BOLD response evoked by foot vibrotactile stimulation: Influence of vibration amplitude and stimulus waveform , 2008, NeuroImage.

[11]  E. Procyk,et al.  The primate working memory networks , 2004, Cognitive, affective & behavioral neuroscience.

[12]  Xiaoping Hu,et al.  Tactile discrimination of grating orientation: fMRI activation patterns , 2005, Human brain mapping.

[13]  Franco Lepore,et al.  Brain activity associated with the electrodermal reactivity to acute heat pain , 2009, NeuroImage.

[14]  Diana J. Vincent,et al.  The Range of Motor Activation in the Normal Human Cortex Using Bold fMRI , 2006, Brain Topography.

[15]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[16]  Michael Petrides,et al.  Ventrolateral prefrontal cortex and tactile memory disambiguation in the human brain , 2007, Proceedings of the National Academy of Sciences.

[17]  Response of SII cortex to ipsilateral, contralateral and bilateral flutter stimulation in the cat , 2005, BMC neuroscience.

[18]  J. Downar,et al.  A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. , 2002, Journal of neurophysiology.

[19]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[20]  P. Pietrini,et al.  Neural correlates of spatial working memory in humans: A functional magnetic resonance imaging study comparing visual and tactile processes , 2006, Neuroscience.

[21]  B. Krauss,et al.  A Comparative fMRI Study of Cortical Representations for Thermal Painful, Vibrotactile, and Motor Performance Tasks , 1999, NeuroImage.

[22]  R. Veit,et al.  BOLD adaptation in vibrotactile stimulation: neuronal networks involved in frequency discrimination. , 2007, Journal of neurophysiology.

[23]  F. Mauguière,et al.  Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. , 2002, Cerebral cortex.

[24]  Guy Marchal,et al.  Passive somatosensory discrimination tasks in healthy volunteers: Differential networks involved in familiar versus unfamiliar shape and length discrimination , 2005, NeuroImage.

[25]  Alan C. Evans,et al.  Attention modulates somatosensory cerebral blood flow response to vibrotactile stimulation as measured by positron emission tomography , 1991, Annals of neurology.

[26]  C. A. Porro,et al.  Touch or pain? Spatio-temporal patterns of cortical fMRI activity following brief mechanical stimuli , 2008, PAIN.

[27]  N. Picard,et al.  Bilateral receptive fields in cortical area SII: contribution of the corpus callosum and other interhemispheric commissures. , 1990, Somatosensory & motor research.

[28]  W. McIlroy,et al.  Tactile stimulus predictability modulates activity in a tactile-motor cortical network , 2003, Experimental Brain Research.

[29]  Harold Burton,et al.  Multiple parietal operculum subdivisions in humans: Tactile activation maps , 2008, Somatosensory & motor research.

[30]  Matthias M. Müller,et al.  Sustained spatial attention to vibration is mediated in primary somatosensory cortex , 2007, NeuroImage.

[31]  J. Girvin,et al.  Cardiovascular effects of human insular cortex stimulation , 1992, Neurology.

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

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

[34]  Maria Blatow,et al.  fMRI reflects functional connectivity of human somatosensory cortex , 2007, NeuroImage.

[35]  Susan J. Lederman,et al.  Multisensory Activation of the Intraparietal Area When Classifying Grating Orientation: A Functional Magnetic Resonance Imaging Study , 2006, The Journal of Neuroscience.

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

[37]  H. Burton,et al.  Cortical activity to vibrotactile stimulation: An fMRI study in blind and sighted individuals , 2004, Human brain mapping.

[38]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

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

[40]  M. Seyal,et al.  Suppression of spatial localization of a cutaneous stimulus following transcranial magnetic pulse stimulation of the sensorimotor cortex. , 1997, Electroencephalography and clinical neurophysiology.

[41]  W. Penfield,et al.  The insula; further observations on its function. , 1955, Brain : a journal of neurology.

[42]  M. Hallett,et al.  Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. , 2008, Cerebral cortex.

[43]  L. Garcia-Larrea,et al.  Timing and characteristics of perceptual attenuation by transcranial stimulation: a study using magnetic cortical stimulation and somatosensory-evoked potentials. , 1999, Psychophysiology.

[44]  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.

[45]  R. Sinclair,et al.  Tactile-spatial and cross-modal attention effects in the primary somatosensory cortical areas 3b and 1-2 of rhesus monkeys , 2000, Somatosensory & motor research.

[46]  W Grodd,et al.  Opposite hemispheric lateralization effects during speaking and singing at motor cortex, insula and cerebellum , 2000, Neuroreport.

[47]  Alan C. Evans,et al.  Propofol anesthesia and cerebral blood flow changes elicited by vibrotactile stimulation: a positron emission tomography study. , 2001, Journal of neurophysiology.

[48]  Fred Tam,et al.  Functional MRI of working memory and selective attention in vibrotactile frequency discrimination , 2007, BMC Neuroscience.

[49]  H. Burton,et al.  Vibrotactile stimulus order effects in somatosensory cortical areas of rhesus monkeys. , 1998, Somatosensory & motor research.

[50]  Arno Villringer,et al.  Neural Correlates of Vibrotactile Working Memory in the Human Brain , 2006, The Journal of Neuroscience.

[51]  Anthony K. P. Jones,et al.  Parietal cortex involvement in the localization of tactile and noxious mechanical stimuli: A transcranial magnetic stimulation study , 2007, Behavioural Brain Research.

[52]  G. Recanzone,et al.  Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task. , 1992, Journal of neurophysiology.

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

[54]  Mark W. Woolrich,et al.  Attention to touch modulates activity in both primary and secondary somatosensory areas. , 2000 .

[55]  B. Whitsel,et al.  Activation of cat SII cortex by flutter stimulation of contralateral vs. ipsilateral forepaws , 2006, Brain Research.

[56]  C Büchel,et al.  Brain regions involved in articulation , 1999, The Lancet.

[57]  Francis McGlone,et al.  Functional neuroimaging studies of human somatosensory cortex , 2002, Behavioural Brain Research.

[58]  Harold Burton,et al.  Cortical network for vibrotactile attention: A fMRI study , 2008, Human brain mapping.

[59]  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.

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

[61]  R. Coghill,et al.  Hemispheric lateralization of somatosensory processing. , 2001, Journal of neurophysiology.

[62]  S. C. Gandevia,et al.  Somatotopic organization of the processing of muscle and cutaneous pain in the left and right insula cortex: A single-trial fMRI study , 2007, Pain.

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

[64]  E. Disbrow,et al.  Somatosensory cortex: A comparison of the response to noxious thermal, mechanical, and electrical stimuli using functional magnetic resonance imaging , 1998, Human brain mapping.

[65]  H Burton,et al.  Tactile-spatial and cross-modal attention effects in the second somatosensory and 7b cortical areas of rhesus monkeys. , 1997, Somatosensory & motor research.

[66]  B. Libet Unconscious cerebral initiative and the role of conscious will in voluntary action , 1985, Behavioral and Brain Sciences.

[67]  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.

[68]  S-J Blakemore,et al.  Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. , 2005, Brain : a journal of neurology.

[69]  W. Medendorp,et al.  Behavioral and cortical mechanisms for spatial coding and action planning , 2008, Cortex.