Oscillatory Correlates of Vibrotactile Frequency Processing in Human Working Memory

Previous animal research has revealed neuronal activity underlying short-term retention of vibrotactile stimuli, providing evidence for a parametric representation of stimulus frequency in primate tactile working memory (Romo et al., 1999). Here, we investigated the neural correlates of vibrotactile frequency processing in human working memory, using noninvasive electroencephalography (EEG). Participants judged the frequencies of vibrotactile stimuli delivered to the fingertip in a delayed match-to-sample frequency discrimination task. As expected, vibrotactile stimulation elicited pronounced steady-state evoked potentials, which were source-localized in primary somatosensory cortex. Furthermore, parametric analysis of induced EEG responses revealed that the frequency of stimulation was reflected by systematic modulations of synchronized oscillatory activity in nonprimary cortical areas. Stimulus processing was accompanied by frequency-dependent alpha-band responses (8–12 Hz) over dorsal occipital cortex. The critical new finding was that, throughout the retention interval, the stimulus frequency held in working memory was systematically represented by a modulation in prefrontal beta activity (20–25 Hz), which was source-localized to the inferior frontal gyrus. This modulation in oscillatory activity during stimulus retention was related to successful frequency discrimination, thus reflecting behaviorally relevant information. Together, the results complement previous findings of parametric working memory correlates in nonhuman primates and suggest that the quantitative representation of vibrotactile frequency in sensory memory entails systematic modulations of synchronized neural activity in human prefrontal cortex.

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

[2]  T. Hendler,et al.  Visuo-haptic object-related activation in the ventral visual pathway , 2001, Nature Neuroscience.

[3]  Karl J. Friston,et al.  Applications of random field theory to electrophysiology , 2005, Neuroscience Letters.

[4]  S. Kiebel,et al.  An Introduction to Random Field Theory , 2003 .

[5]  Anthony D. Cate,et al.  Auditory Attention Activates Peripheral Visual Cortex , 2009, PloS one.

[6]  R. Oostenveld,et al.  Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas , 2006, The Journal of Neuroscience.

[7]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[8]  J. Pardo,et al.  Aversive gustatory stimulation activates limbic circuits in humans. , 1998, Brain : a journal of neurology.

[9]  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 .

[10]  Christian Gerloff,et al.  Larger interregional synchrony is associated with greater behavioral success in a complex sensory integration task in humans. , 2005, Cerebral cortex.

[11]  N. Logothetis,et al.  Frequency-Band Coupling in Surface EEG Reflects Spiking Activity in Monkey Visual Cortex , 2009, Neuron.

[12]  T. Pasternak,et al.  Working memory in primate sensory systems , 2005, Nature Reviews Neuroscience.

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

[14]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[15]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

[16]  N. Costes,et al.  Haemodynamic brain responses to acute pain in humans: sensory and attentional networks. , 1999, Brain : a journal of neurology.

[17]  R. Romo,et al.  Periodicity and Firing Rate As Candidate Neural Codes for the Frequency of Vibrotactile Stimuli , 2000, The Journal of Neuroscience.

[18]  David H Zald,et al.  Somatosensory processing in the human inferior prefrontal cortex. , 2002, Journal of neurophysiology.

[19]  M Schwaiger,et al.  Processing of histamine-induced itch in the human cerebral cortex: a correlation analysis with dermal reactions. , 2000, The Journal of investigative dermatology.

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

[21]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[22]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[23]  Juha Virtanen,et al.  Activation of multiple cortical areas in response to somatosensory stimulation: Combined magnetoencephalographic and functional magnetic resonance imaging , 1999, Human brain mapping.

[24]  G. Pfurtscheller,et al.  Event-related cortical desynchronization detected by power measurements of scalp EEG. , 1977, Electroencephalography and clinical neurophysiology.

[25]  E. Reiman,et al.  Thermosensory activation of insular cortex , 2000, Nature Neuroscience.

[26]  Shozo Tobimatsu,et al.  Steady-state vibration somatosensory evoked potentials: physiological characteristics and tuning function , 1999, Clinical Neurophysiology.

[27]  Markus Siegel,et al.  Phase-dependent neuronal coding of objects in short-term memory , 2009, Proceedings of the National Academy of Sciences.

[28]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[29]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[30]  R. Romo,et al.  Neural codes for perceptual discrimination in primary somatosensory cortex , 2005, Nature Neuroscience.

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

[32]  E. Rolls,et al.  The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. , 1999, Neuroreport.

[33]  Karl J. Friston,et al.  Bayesian estimation of evoked and induced responses , 2006, Human brain mapping.

[34]  K. Carlsson,et al.  Tickling Expectations: Neural Processing in Anticipation of a Sensory Stimulus , 2000, Journal of Cognitive Neuroscience.

[35]  R. Romo,et al.  Neuronal correlates of decision-making in secondary somatosensory cortex , 2002, Nature Neuroscience.

[36]  Hauke R. Heekeren,et al.  What Happens in Between? Human Oscillatory Brain Activity Related to Crossmodal Spatial Cueing , 2008, PloS one.

[37]  Justin A. Harris,et al.  Transient Storage of a Tactile Memory Trace in Primary Somatosensory Cortex , 2002, The Journal of Neuroscience.

[38]  M. Mesulam.  Attentional networks, confusional states, and neglect syndromes. , 2000 .

[39]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[40]  W. Klimesch,et al.  Oscillatory mechanisms of process binding in memory , 2010, Neuroscience & Biobehavioral Reviews.

[41]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

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

[43]  R. Romo,et al.  Frequency discrimination in the sense of flutter: psychophysical measurements correlated with postcentral events in behaving monkeys , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  A. Nobre,et al.  The Large-Scale Neural Network for Spatial Attention Displays Multifunctional Overlap But Differential Asymmetry , 1999, NeuroImage.

[45]  H. Barbas.  Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey , 1988, The Journal of comparative neurology.

[46]  J. Palva,et al.  New vistas for alpha-frequency band oscillations. , 2007, Trends in neurosciences.

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

[48]  Fred Tam,et al.  Magnetoencephalographic study of vibrotactile evoked transient and steady-state responses in human somatosensory cortex , 2006, NeuroImage.

[49]  R. Koeppe,et al.  Anatomic standardization: linear scaling and nonlinear warping of functional brain images. , 1994, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[50]  R. Oostenveld,et al.  Somatosensory working memory performance in humans depends on both engagement and disengagement of regions in a distributed network , 2009, Human brain mapping.

[51]  Stefan J Kiebel,et al.  Parametric analysis of oscillatory activity as measured with EEG/MEG , 2005, Human brain mapping.

[52]  S. Stone-Elander,et al.  Pain-related cerebral activation is altered by a distracting cognitive task , 2000, Pain.

[53]  Dani Byrd,et al.  Auditory Selective Attention: An fMRI Investigation , 1996, NeuroImage.

[54]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.

[55]  J. Palva,et al.  New vistas for α-frequency band oscillations , 2007, Trends in Neurosciences.

[56]  G. Pfurtscheller,et al.  ERD/ERS patterns reflecting sensorimotor activation and deactivation. , 2006, Progress in brain research.

[57]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[58]  Michael Petrides,et al.  Three-Dimensional Probabilistic Atlas of the Human Orbitofrontal Sulci in Standardized Stereotaxic Space , 2001, NeuroImage.

[59]  C. Robinson,et al.  Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis , 1980, The Journal of comparative neurology.

[60]  Tony Ro,et al.  Human MST But Not MT Responds to Tactile Stimulation , 2007, The Journal of Neuroscience.

[61]  Karl J. Friston,et al.  Electromagnetic source reconstruction for group studies , 2008, NeuroImage.