Steady-state evoked potentials to study the processing of tactile and nociceptive somatosensory input in the human brain

The periodic presentation of a sensory stimulus induces, at certain frequencies of stimulation, a sustained electroencephalographic response of corresponding frequency, known as steady-state evoked potentials (SS-EP). In visual, auditory and vibrotactile modalities, studies have shown that SS-EP reflect mainly activity originating from early, modality-specific sensory cortices. Furthermore, it has been shown that SS-EP have several advantages over the recording of transient event-related brain potentials (ERP), such as a high signal-to-noise ratio, a shorter time to obtain reliable signals, and the capacity to frequency-tag the cortical activity elicited by concurrently presented sensory stimuli. Recently, we showed that SS-EP can be elicited by the selective activation of skin nociceptors and that nociceptive SS-EP reflect the activity of a population of neurons that is spatially distinct from the somatotopically-organized population of neurons underlying vibrotactile SS-EP. Hence, the recording of SS-EP offers a unique opportunity to study the cortical representation of nociception and touch in humans, and to explore their potential crossmodal interactions. Here, (1) we review available methods to achieve the rapid periodic stimulation of somatosensory afferents required to elicit SS-EP, (2) review previous studies that have characterized vibrotactile and nociceptive SS-EP, (3) discuss the nature of the recorded signals and their relationship with transient event-related potentials and (4) outline future perspectives and potential clinical applications of this technique.

[1]  R. Lemon,et al.  EEG oscillations at 600 Hz are macroscopic markers for cortical spike bursts , 2003, The Journal of physiology.

[2]  J. Gross,et al.  Steady-State Visual Evoked Potentials Can Be Explained by Temporal Superposition of Transient Event-Related Responses , 2011, PloS one.

[3]  C. Yingling,et al.  Steady-state analysis of somatosensory evoked potentials. , 1996, Electroencephalography and clinical neurophysiology.

[4]  Matthias M. Müller,et al.  Sustained selective intermodal attention modulates processing of language-like stimuli , 2011, Experimental Brain Research.

[5]  A. Cichocki,et al.  Steady-state visually evoked potentials: Focus on essential paradigms and future perspectives , 2010, Progress in Neurobiology.

[6]  A. Mouraux,et al.  Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. , 2009, Journal of neurophysiology.

[7]  Matthias M. Müller,et al.  Shift of attention to the body location of distracters is mediated by perceptual load in sustained somatosensory attention , 2009, Biological Psychology.

[8]  O. Ozdamar,et al.  Methodology to Estimate the Transient Evoked Responses for the Generation of Steady State Responses , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[9]  S. Hillyard,et al.  Selective attention to stimulus location modulates the steady-state visual evoked potential. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Kenneth O. Johnson,et al.  The roles and functions of cutaneous mechanoreceptors , 2001, Current Opinion in Neurobiology.

[11]  J Ellrich,et al.  A new method to increase nociception specificity of the human blink reflex , 2000, Clinical Neurophysiology.

[12]  T Imada,et al.  Human somatosensory evoked magnetic fields to vibratory stimulation of the index finger: is there frequency organization in SI? , 1998, Electroencephalography and clinical neurophysiology.

[13]  J. Farquhar,et al.  Transient and steady-state responses to mechanical stimulation of different fingers reveal interactions based on lateral inhibition , 2010, Clinical Neurophysiology.

[14]  Maurizio Maurizi,et al.  Generation of human auditory steady-state responses (SSRs). II: Addition of responses to individual stimuli , 1995, Hearing Research.

[15]  P. Strick,et al.  The Spinothalamic System Targets Motor and Sensory Areas in the Cerebral Cortex of Monkeys , 2009, The Journal of Neuroscience.

[16]  A. Mouraux,et al.  Nociceptive Steady-State Evoked Potentials Elicited by Rapid Periodic Thermal Stimulation of Cutaneous Nociceptors , 2011, The Journal of Neuroscience.

[17]  Guido Conti,et al.  Auditory steady-state responses to click trains from the rat temporal cortex , 1999, Clinical Neurophysiology.

[18]  R. Meyer,et al.  Secondary hyperalgesia to punctate mechanical stimuli. Central sensitization to A-fibre nociceptor input. , 1999, Brain : a journal of neurology.

[19]  André Mouraux,et al.  Steady-state evoked potentials to tag specific components of nociceptive cortical processing , 2012, NeuroImage.

[20]  S. Makeig,et al.  A 40-Hz auditory potential recorded from the human scalp. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. Kakigi,et al.  Preferential stimulation of Aδ fibers by intra-epidermal needle electrode in humans , 2002, Pain.

[22]  D. Regan,et al.  An audio-visual convergence area in the human brain , 2004, Experimental Brain Research.

[23]  M. Nolano,et al.  Topical capsaicin in humans: parallel loss of epidermal nerve fibers and pain sensation , 1999, Pain.

[24]  S. Folger,et al.  EEG evidence of stimulus-directed response dynamics in human somatosensory cortex , 1999, Brain Research.

[25]  A. Mouraux,et al.  Low intensity intra-epidermal electrical stimulation can activate Aδ-nociceptors selectively , 2010, PAIN.

[26]  Francesco Sala,et al.  Steady-state activation in somatosensory cortex after changes in stimulus rate during median nerve stimulation. , 2009, Magnetic resonance imaging.

[27]  M. Frot,et al.  Brain generators of laser-evoked potentials: from dipoles to functional significance , 2003, Neurophysiologie Clinique/Clinical Neurophysiology.

[28]  Jorge Bohórquez,et al.  Generation of the 40-Hz auditory steady-state response (ASSR) explained using convolution , 2008, Clinical Neurophysiology.

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

[30]  D. P. Russell,et al.  Increased Synchronization of Neuromagnetic Responses during Conscious Perception , 1999, The Journal of Neuroscience.

[31]  Alfons Schnitzler,et al.  Rapid mapping of finger representations in human primary somatosensory cortex applying neuromagnetic steady-state responses , 2002, Neuroreport.

[32]  D. Kenshalo,et al.  A device to measure cutaneous temperature sensitivity in humans and subhuman species. , 1975, Journal of applied physiology.

[33]  Walter Magerl,et al.  C- and Aδ-fiber components of heat-evoked cerebral potentials in healthy human subjects , 1999, Pain.

[34]  Isabelle Peretz,et al.  Steady-state evoked potentials as an index of multisensory temporal binding , 2012, NeuroImage.

[35]  A. Apkarian,et al.  Cortical representation of pain: functional characterization of nociceptive areas near the lateral sulcus , 2000, Pain.

[36]  Robert Galambos,et al.  TACTILE AND AUDITORY STIMULI REPEATED AT HIGH RATES (30–50 PER SEC) PRODUCE SIMILAR EVENT RELATED POTENTIALS * , 1980 .

[37]  Guido Conti,et al.  Generation of human auditory steady-state responses , 1998 .

[38]  D. Stuart,et al.  Thermal electrodes based on "Peltier effect". , 1962, Electroencephalography and clinical neurophysiology.

[39]  J. Driver,et al.  Multisensory Interplay Reveals Crossmodal Influences on ‘Sensory-Specific’ Brain Regions, Neural Responses, and Judgments , 2008, Neuron.

[40]  E. Valentini,et al.  Cognitive aspects of nociception and pain. Bridging neurophysiology with cognitive psychology , 2012, Neurophysiologie Clinique/Clinical Neurophysiology.

[41]  A. Mouraux,et al.  Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? , 2008, Journal of neurophysiology.

[42]  H. Berger.  Über das Elektrenkephalogramm des Menschen , 1929, Archiv für Psychiatrie und Nervenkrankheiten.

[43]  Matthias M. Müller,et al.  Effects of spatial selective attention on the steady-state visual evoked potential in the 20-28 Hz range. , 1998, Brain research. Cognitive brain research.

[44]  G. Pfurtscheller,et al.  „Resonance-like“ Frequencies of Sensorimotor Areas Evoked by Repetitive Tactile Stimulation - Resonanzeffekte in sensomotorischen Arealen, evoziert durch rhythmische taktile Stimulation , 2001, Biomedizinische Technik. Biomedical engineering.

[45]  Peter Praamstra,et al.  Movement-related changes in cortical excitability: A steady-state SEP approach , 2008, Brain Research.

[46]  C. Herrmann.  Human EEG responses to 1–100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena , 2001, Experimental Brain Research.

[47]  Matthias M. Müller,et al.  Human Neuroscience , 2022 .

[48]  Rolf-Detlef Treede,et al.  Laser-evoked potentials are graded and somatotopically organized anteroposteriorly in the operculoinsular cortex of anesthetized monkeys. , 2006, Journal of neurophysiology.

[49]  Winfried Schlee,et al.  Top-Down Modulation of the Auditory Steady-State Response in a Task-Switch Paradigm , 2008, Front. Hum. Neurosci..

[50]  L. Garcia-Larrea,et al.  Contribution of attentional and cognitive factors to laser evoked brain potentials , 2003, Neurophysiologie Clinique/Clinical Neurophysiology.

[51]  Randall J. Nelson,et al.  High-frequency vibratory sensitive neurons in monkey primary somatosensory cortex: entrained and nonentrained responses to vibration during the performance of vibratory-cued hand movements , 1996, Experimental Brain Research.

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

[53]  S A Hillyard,et al.  Feature-selective attention enhances color signals in early visual areas of the human brain , 2006, Proceedings of the National Academy of Sciences.

[54]  T Suzuki,et al.  Effect of natural sleep on auditory steady state responses in adult subjects with normal hearing. , 1994, Audiology : official organ of the International Society of Audiology.

[55]  D. Regan,et al.  Human brain electrophysiology , 1989 .

[56]  Fabrizio De Vico Fallani,et al.  Brain activity during the memorization of visual scenes from TV commercials: An application of high resolution EEG and steady state somatosensory evoked potentials technologies , 2009, Journal of Physiology-Paris.

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

[58]  D. Regan.  Human brain electrophysiology: Evoked potentials and evoked magnetic fields in science and medicine , 1989 .

[59]  S. Martens,et al.  Using frequency tagging to quantify attentional deployment in a visual divided attention task. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[60]  B Bromm,et al.  Late somatosensory evoked cerebral potentials in response to cutaneous heat stimuli. , 1988, Electroencephalography and clinical neurophysiology.

[61]  M. Woldorff,et al.  Attentional capacity for processing concurrent stimuli is larger across sensory modalities than within a modality. , 2006, Psychophysiology.

[62]  Maurizio Maurizi,et al.  Generation of human auditory steadystate responses (SSRs). I: Stimulus rate effects , 1995, Hearing Research.

[63]  T. Elbert,et al.  Specific tonotopic organizations of different areas of the human auditory cortex revealed by simultaneous magnetic and electric recordings. , 1995, Electroencephalography and clinical neurophysiology.

[64]  E. Macaluso,et al.  Multisensory spatial interactions: a window onto functional integration in the human brain , 2005, Trends in Neurosciences.

[65]  A. Carmon,et al.  Evoked cerebral responses to noxious thermal stimuli in humans , 1976, Experimental Brain Research.

[66]  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.

[67]  A Z Snyder,et al.  Steady-state vibration evoked potentials: descriptions of technique and characterization of responses. , 1992, Electroencephalography and clinical neurophysiology.

[68]  A. Mouraux,et al.  The pain matrix reloaded A salience detection system for the body , 2011, Progress in Neurobiology.

[69]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[70]  C. Pantev,et al.  Tonotopic organization of the sources of human auditory steady-state responses , 1996, Hearing Research.

[71]  Shozo Tobimatsu,et al.  Differential temporal coding of the vibratory sense in the hand and foot in man , 2000, Clinical Neurophysiology.

[72]  M Hämäläinen,et al.  Neuromagnetic steady-state responses to auditory stimuli. , 1989, The Journal of the Acoustical Society of America.

[73]  Domenica Le Pera,et al.  Dipolar modelling of the scalp evoked potentials to painful contact heat stimulation of the human skin , 2002, Neuroscience Letters.

[74]  Timothy Bardouille,et al.  MEG imaging of sensorimotor areas using inter-trial coherence in vibrotactile steady-state responses , 2008, NeuroImage.

[75]  Paolo Toffanin,et al.  by steady-state responses in auditory-visual divided attention , 2009 .

[76]  P. M. Rossini,et al.  Recommendations for the clinical use of somatosensory-evoked potentials , 2008, Clinical Neurophysiology.

[77]  D. P. Russell,et al.  Investigating neural correlates of conscious perception by frequency-tagged neuromagnetic responses. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[78]  Anthony K. P. Jones,et al.  The cortical representation of pain , 1999, PAIN.

[79]  M. Bach,et al.  On the statistical significance of electrophysiological steady-state responses , 2004, Documenta Ophthalmologica.

[80]  O. Bertrand,et al.  Effects of Selective Attention on the Electrophysiological Representation of Concurrent Sounds in the Human Auditory Cortex , 2007, The Journal of Neuroscience.

[81]  Matthias M. Müller,et al.  Selective spatial attention to left or right hand flutter sensation modulates the steady-state somatosensory evoked potential. , 2004, Brain research. Cognitive brain research.