Cortical inhibition of laser pain and laser‐evoked potentials by non‐nociceptive somatosensory input

Although the inhibitory action that tactile stimuli can have on pain is well documented, the precise timing of the interaction between the painful and non‐painful stimuli in the central nervous system is unclear. The aim of this study was to investigate this issue by measuring the timing of the amplitude modulation of laser evoked potentials (LEPs) due to conditioning non‐painful stimuli. LEPs were recorded from 31 scalp electrodes in 10 healthy subjects after painful stimulation of the right arm (C6–C7 dermatomes). Non‐painful electrical stimuli were applied by ring electrodes on the second and third finger of the right hand. Electrical stimuli were delivered at +50, +150, +200 and +250 ms interstimulus intervals (ISIs) after the laser pulses. LEPs obtained without any conditioning stimulation were used as a baseline. As compared to the baseline, non‐painful electrical stimulation reduced the amplitude of the vertex N2/P2 LEP component and the laser pain rating when electrical stimuli followed the laser pulses only at +150 and +200 ms ISIs. As at these ISIs the collision between the non‐painful and painful input is likely to take place at the cortical level, we can conclude that the late processing of painful (thermal) stimuli is partially inhibited by the processing of non‐painful (cutaneous) stimuli within the cerebral cortex. Moreover, our results do not provide evidence that non‐painful inputs can inhibit pain at a lower level, including the spinal cord.

[1]  François Mauguière,et al.  Dual representation of pain in the operculo-insular cortex in humans. , 2003, Brain : a journal of neurology.

[2]  L. Arendt-Nielsen Characteristics, detection, and modulation of laser‐evoked vertex potentials , 1994, Acta anaesthesiologica Scandinavica. Supplementum.

[3]  Cortical processing of noxious information in humans: a magnetoencephalographic study. , 2006, Supplements to Clinical neurophysiology.

[4]  Y. Sarne,et al.  Correlation of subjective pain experience with cerebral evoked responses to noxious thermal stimulations , 1978, Experimental Brain Research.

[5]  R. Lesser,et al.  Painful stimuli evoke potentials recorded from the parasylvian cortex in humans. , 1998, Journal of neurophysiology.

[6]  B. Komisaruk,et al.  Nociceptive responses to altered GABAergic activity at the spinal cord. , 1986, Life sciences.

[7]  R. Treede,et al.  Nerve fibre discharges, cerebral potentials and sensations induced by CO2 laser stimulation. , 1984, Human neurobiology.

[8]  C. Coronel,et al.  Transcutaneous electrical nerve stimulation after thoracic surgery: systematic review and meta-analysis of 11 randomized trials. , 2012, Revista brasileira de cirurgia cardiovascular : orgao oficial da Sociedade Brasileira de Cirurgia Cardiovascular.

[9]  P. Wall,et al.  Pain mechanisms: a new theory. , 1965, Science.

[10]  Luis Garcia-Larrea,et al.  Somatosensory volleys and cortical evoked potentials: ‘First come, first served’? , 2004, Pain.

[11]  J. Neilson,et al.  Transcutaneous electrical nerve stimulation (TENS) for pain relief in labour. , 2009, The Cochrane database of systematic reviews.

[12]  Evon M. O. Abu-Taieh,et al.  Comparative study , 2003, BMJ : British Medical Journal.

[13]  B. Pomeranz Specific nociceptive fibers projecting from spinal cord neurons to the brain: a possible pathway for pain. , 1973, Brain research.

[14]  Gonzalo Yevenes,et al.  Fast synaptic inhibition in spinal sensory processing and pain control. , 2012, Physiological reviews.

[15]  Rolf-Detlef Treede,et al.  Dipole source analysis of laser-evoked subdural potentials recorded from parasylvian cortex in humans. , 2003, Journal of neurophysiology.

[16]  H Shibasaki,et al.  Mechanisms of pain relief by vibration and movement. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[17]  J. Sawynok GABAergic mechanisms of analgesia: An update , 1987, Pharmacology Biochemistry and Behavior.

[18]  R. Plentz,et al.  Estimulação elétrica nervosa transcutânea no pós-operatório de cirurgia torácica: revisão sistemática e metanálise de estudos randomizados , 2012 .

[19]  M. Tramèr,et al.  Transcutaneous electrical nerve stimulation (TENS) for chronic pain. , 2000, The Cochrane database of systematic reviews.

[20]  K L Casey,et al.  Variability of laser-evoked potentials: attention, arousal and lateralized differences. , 1993, Electroencephalography and clinical neurophysiology.

[21]  R. Treede,et al.  Equivalent electrical source analysis of pain-related somatosensory evoked potentials elicited by a CO2 laser. , 1993, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[22]  Jhi-Joung Wang,et al.  High-Frequency Transcutaneous Electrical Nerve Stimulation Attenuates Postsurgical Pain and Inhibits Excess Substance P in Rat Dorsal Root Ganglion , 2013, Regional Anesthesia & Pain Medicine.

[23]  A. Schnitzler,et al.  Differential coding of pain intensity in the human primary and secondary somatosensory cortex. , 2001, Journal of neurophysiology.

[24]  L. Sousa,et al.  Transcutaneous electrical nerve stimulation for the relief of post‐partum uterine contraction pain during breast‐feeding: A randomized clinical trial , 2014, The journal of obstetrics and gynaecology research.

[25]  G. Osmond,et al.  Coadministration of intrathecal strychnine and bicuculline effects synergistic allodynia in the rat: an isobolographic analysis. , 2001, The Journal of pharmacology and experimental therapeutics.

[26]  M. Frot,et al.  Do we activate specifically somatosensory thin fibres with the concentric planar electrode? A scalp and intracranial EEG study , 2012, PAIN.

[27]  F. Mauguière,et al.  Intracortical recordings of early pain-related CO2-laser evoked potentials in the human second somatosensory (SII) area , 1999, Clinical Neurophysiology.

[28]  Mark I. Johnson,et al.  Transcutaneous electrical nerve stimulation for the management of painful conditions: focus on neuropathic pain , 2011, Expert review of neurotherapeutics.

[29]  R. Melzack The gate control theory of pain. , 1978, British medical journal.

[30]  U. Baumgärtner,et al.  Clinical usefulness of laser-evoked potentials , 2003, Neurophysiologie Clinique/Clinical Neurophysiology.

[31]  P. Livrea,et al.  A comparative study of cortical responses evoked by transcutaneous electrical vs CO2 laser stimulation , 2011, Clinical Neurophysiology.

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

[33]  A. Dickenson,et al.  The pharmacology of excitatory and inhibitory amino acid-mediated events in the transmission and modulation of pain in the spinal cord. , 1997, General pharmacology.

[34]  J. Spiegel,et al.  Laser-evoked potentials after painful hand and foot stimulation in humans: evidence for generation of the middle-latency component in the secondary somatosensory cortex , 1996, Neuroscience Letters.

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

[36]  C. Woolf,et al.  The contribution of GABAA and glycine receptors to central sensitization: disinhibition and touch-evoked allodynia in the spinal cord. , 1994, Journal of neurophysiology.

[37]  F. Mauguière,et al.  Scalp topography and dipolar source modelling of potentials evoked by CO2 laser stimulation of the hand. , 1996, Electroencephalography and clinical neurophysiology.

[38]  D. Bentley,et al.  Anatomical localization and intra-subject reproducibility of laser evoked potential source in cingulate cortex, using a realistic head model , 2002, Clinical Neurophysiology.

[39]  R. Treede,et al.  Topography of middle-latency somatosensory evoked potentials following painful laser stimuli and non-painful electrical stimuli. , 1993, Electroencephalography and clinical neurophysiology.

[40]  F. Mauguière,et al.  Sources of cortical responses to painful CO2 laser skin stimulation of the hand and foot in the human brain , 2000, Clinical Neurophysiology.

[41]  A. Chen,et al.  Brain electrical source analysis of laser evoked potentials in response to painful trigeminal nerve stimulation. , 1995, Electroencephalography and clinical neurophysiology.

[42]  P. Nathan The gate-control theory of pain. A critical review. , 1976, Brain : a journal of neurology.

[43]  N. Bowery,et al.  GABA and its receptors in the spinal cord. , 1996, Trends in pharmacological sciences.

[44]  L. Epstein,et al.  Managing chronic pain with spinal cord stimulation. , 2012, The Mount Sinai journal of medicine, New York.

[45]  A. Basbaum,et al.  Transmitting Pain and Itch Messages: A Contemporary View of the Spinal Cord Circuits that Generate Gate Control , 2014, Neuron.

[46]  Zizhen Zhang,et al.  Topical bicuculline to the rat spinal cord induces highly localized allodynia that is mediated by spinal prostaglandins , 2001, PAIN®.

[47]  F. Porreca,et al.  Spinal GABA(A) and GABA(B) receptor pharmacology in a rat model of neuropathic pain. , 2002, Anesthesiology.

[48]  N E Crone,et al.  Cutaneous painful laser stimuli evoke responses recorded directly from primary somatosensory cortex in awake humans. , 2004, Journal of neurophysiology.

[49]  P. D. Wall,et al.  The gate control theory of pain mechanisms. A re-examination and re-statement. , 1978 .

[50]  F. Mauguière,et al.  Association and dissociation between laser‐evoked potentials and pain perception , 1997, Neuroreport.

[51]  L. Sorkin,et al.  Spinal bicuculline produces hypersensitivity of dorsal horn neurons: effects of excitatory amino acid antagonists , 1998, Pain.

[52]  J. Ellrich,et al.  Peripheral Nerve Stimulation Inhibits Nociceptive Processing: An Electrophysiological Study in Healthy Volunteers , 2005, Neuromodulation : journal of the International Neuromodulation Society.

[53]  L. Mendell Constructing and deconstructing the gate theory of pain , 2014, PAIN®.