Parallel Processing of Nociceptive A-δ Inputs in SII and Midcingulate Cortex in Humans

The cingulate cortex (CC) as a part of the “medial” pain subsystem is generally assumed to be involved in the affective and/or cognitive dimensions of pain processing, which are viewed as relatively slow processes compared with the sensory-discriminative pain coding by the lateral second somatosensory area (SII)–insular cortex. The present study aimed at characterizing the location and timing of the CC evoked responses during the 1 s period after a painful laser stimulus, by exploring the whole rostrocaudal extent of this cortical area using intracortical recordings in humans. Only a restricted area in the median CC region responded to painful stimulation, namely the posterior midcingulate cortex (pMCC), the location of which is consistent with the so-called “motor CC” in monkeys. Cingulate pain responses showed two components, of which the earliest peaked at latencies similar to those obtained in SII. These data provide direct evidence that activations underlying the processing of nociceptive information can occur simultaneously in the “medial” and “lateral” subsystems. The existence of short-latency pMCC responses to pain further indicates that the “medial pain system” is not devoted exclusively to the processing of emotional information, but is also involved in fast attentional orienting and motor withdrawal responses to pain inputs. These functions are, not surprisingly, conducted in parallel with pain intensity coding and stimulus localization specifically subserved by the sensory-discriminative “lateral” pain system.

[1]  F. Mauguière,et al.  Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study , 2008, Clinical Neurophysiology.

[2]  V. Legrain,et al.  Laser evoked responses to painful stimulation persist during sleep and predict subsequent arousals , 2008, PAIN®.

[3]  Gereon R Fink,et al.  The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. , 2007, Cerebral cortex.

[4]  C. Kennard,et al.  The role of the pre-supplementary motor area in the control of action , 2007, NeuroImage.

[5]  David W. McNeal,et al.  Amygdala interconnections with the cingulate motor cortex in the rhesus monkey , 2007, The Journal of comparative neurology.

[6]  F Mauguière,et al.  Somatosensory and pain responses to stimulation of the second somatosensory area (SII) in humans. A comparison with SI and insular responses. , 2006, Cerebral cortex.

[7]  K. Amunts,et al.  The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. , 2006, Cerebral cortex.

[8]  A. Schleicher,et al.  The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. , 2006, Cerebral cortex.

[9]  B. Vogt Pain and emotion interactions in subregions of the cingulate gyrus , 2005, Nature Reviews Neuroscience.

[10]  Karl J. Friston,et al.  Attention to pain localization and unpleasantness discriminates the functions of the medial and lateral pain systems , 2005, The European journal of neuroscience.

[11]  Rolf-Detlef Treede,et al.  Spatial resolution of fMRI in the human parasylvian cortex: Comparison of somatosensory and auditory activation , 2005, NeuroImage.

[12]  Yu-Te Wu,et al.  Spatiotemporal brain dynamics in response to muscle stimulation , 2005, NeuroImage.

[13]  J. Lorenz,et al.  Imaging of acute versus pathological pain in humans , 2005, European journal of pain.

[14]  J. Greenspan,et al.  Studies of the human ascending pain pathways , 2005 .

[15]  A. Mouraux,et al.  Refractoriness cannot explain why C-fiber laser-evoked brain potentials are recorded only if concomitant Aδ-fiber activation is avoided , 2004, Pain.

[16]  N. Crone,et al.  Amplitudes of laser evoked potential recorded from primary somatosensory, parasylvian and medial frontal cortex are graded with stimulus intensity , 2004, Pain.

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

[18]  Burkhart Bromm,et al.  The involvement of the posterior cingulate gyrus in phasic pain processing of humans , 2004, Neuroscience Letters.

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

[20]  B. Vogt,et al.  Structural and functional dichotomy of human midcingulate cortex , 2003, The European journal of neuroscience.

[21]  G Cruccu,et al.  Unmyelinated trigeminal pathways as assessed by laser stimuli in humans. , 2003, Brain : a journal of neurology.

[22]  Walter Magerl,et al.  Left-hemisphere dominance in early nociceptive processing in the human parasylvian cortex , 2003, NeuroImage.

[23]  Ewald Moser,et al.  The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response , 2003, NeuroImage.

[24]  Naomi Hasegawa,et al.  Thalamocortical and intracortical connections of monkey cingulate motor areas , 2003, The Journal of comparative neurology.

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

[26]  Joachim Gross,et al.  Cortical representation of first and second pain sensation in humans , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Derbyshire,et al.  Functional imaging of pain perception , 2002, Current rheumatology reports.

[28]  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.

[29]  C. Büchel,et al.  Dissociable Neural Responses Related to Pain Intensity, Stimulus Intensity, and Stimulus Awareness within the Anterior Cingulate Cortex: A Parametric Single-Trial Laser Functional Magnetic Resonance Imaging Study , 2002, The Journal of Neuroscience.

[30]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[31]  F. Mauguière,et al.  Responses of the supra-sylvian (SII) cortex in humans to painful and innocuous stimuli A study using intra-cerebral recordings , 2001, Pain.

[32]  M. Bushnell,et al.  Cortical representation of the sensory dimension of pain. , 2001, Journal of neurophysiology.

[33]  R. Treede,et al.  Inactivation and tachyphylaxis of heat‐evoked inward currents in nociceptive primary sensory neurones of rats , 2000, The Journal of physiology.

[34]  F. Mauguière,et al.  The role of the insular cortex in temporal lobe epilepsy , 2000, Annals of neurology.

[35]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[36]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

[37]  L. Krubitzer,et al.  Somatotopic organization of cortical fields in the lateral sulcus of Homo sapiens: Evidence for SII and PV , 2000, The Journal of comparative neurology.

[38]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[39]  F. Mauguière,et al.  Timing and spatial distribution of somatosensory responses recorded in the upper bank of the sylvian fissure (SII area) in humans. , 1999, Cerebral cortex.

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

[41]  R. Treede,et al.  Direct evidence of nociceptive input to human anterior cingulate gyrus and parasylvian cortex , 1999, Current review of pain.

[42]  A Schnitzler,et al.  Pain affect without pain sensation in a patient with a postcentral lesion , 1999, Pain.

[43]  J. Dostrovsky,et al.  Pain-related neurons in the human cingulate cortex , 1999, Nature Neuroscience.

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

[45]  B Conrad,et al.  Region‐specific encoding of sensory and affective components of pain in the human brain: A positron emission tomography correlation analysis , 1999, Annals of neurology.

[46]  T. Talaieva,et al.  [The role of a systemic inflammatory process in the atherogenic modification of lipoproteins and the development of hypercholesterolemia]. , 1999, Fiziolohichnyi zhurnal.

[47]  R. Morecraft,et al.  Convergence of Limbic Input to the Cingulate Motor Cortex in the Rhesus Monkey , 1998, Brain Research Bulletin.

[48]  R P Lesser,et al.  Painful stimuli evoke potentials recorded over the human anterior cingulate gyrus. , 1998, Journal of neurophysiology.

[49]  R. Kakigi,et al.  Simple and novel method for measuring conduction velocity of A delta fibers in humans. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[50]  M. Bushnell,et al.  Pain affect encoded in human anterior cingulate but not somatosensory cortex. , 1997, Science.

[51]  Richard S. J. Frackowiak,et al.  Multiple nonprimary motor areas in the human cortex. , 1997, Journal of neurophysiology.

[52]  W. Willis,et al.  Neuroanatomy of the pain system and of the pathways that modulate pain. , 1997, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[53]  K. Iwata,et al.  Morphological and electrophysiological properties of ACCx nociceptive neurons in rats , 1996, Brain Research.

[54]  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.

[55]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[56]  C. Asanuma,et al.  Neurobiology of Cingulate Cortex and Limbic Thalamus edited by B. A. Vogt and M. Gabriel, Birkha¨user, 1993. $199.00 (639 pages) ISBN 0 8176 3568 8 , 1994, Trends in Neurosciences.

[57]  G. V. Van Hoesen,et al.  Frontal granular cortex input to the cingulate (M3), supplementary (M2) and primary (M1) motor cortices in the rhesus monkey , 1993, The Journal of comparative neurology.

[58]  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.

[59]  M. Gabriel,et al.  Neurobiology of Cingulate Cortex and Limbic Thalamus , 1993 .

[60]  B. Vogt,et al.  Nociceptive neurons in area 24 of rabbit cingulate cortex. , 1992, Journal of neurophysiology.

[61]  G. V. Van Hoesen,et al.  Cingulate input to the primary and supplementary motor cortices in the rhesus monkey: Evidence for somatotopy in areas 24c and 23c , 1992, The Journal of comparative neurology.

[62]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  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 .

[64]  C J Hodge,et al.  Primate spinothalamic pathways: I. A quantitative study of the cells of origin of the spinothalamic pathway , 1989, The Journal of comparative neurology.

[65]  D. Pandya,et al.  Cingulate cortex of the rhesus monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

[66]  K. Berkley,et al.  Diencephalic mechanisms of pain sensation , 1985, Brain Research Reviews.

[67]  J. Gybels,et al.  Response properties of thin myelinated (A-delta) fibers in human skin nerves. , 1983, Journal of neurophysiology.

[68]  J. Fermaglich Electric Fields of the Brain: The Neurophysics of EEG , 1982 .

[69]  F Mauguiere,et al.  The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis. , 1980, Brain : a journal of neurology.

[70]  William D. Willis,et al.  The cells of origin of the primate spinothalamic tract , 1979, The Journal of comparative neurology.

[71]  W. K. Dong,et al.  Nociceptive responses of neurons in medial thalamus and their relationship to spinothalamic pathways. , 1978, Journal of neurophysiology.

[72]  K. Casey Unit analysis of nociceptive mechanisms in the thalamus of the awake squirrel monkey. , 1966, Journal of neurophysiology.

[73]  E L FOLTZ,et al.  Pain "relief" by frontal cingulumotomy. , 1962, Journal of neurosurgery.