Somatosensory and pain responses to stimulation of the second somatosensory area (SII) in humans. A comparison with SI and insular responses.

Somatosensory and pain responses to direct intracerebral stimulations of the SII area were obtained in 14 patients referred for epilepsy surgery. Stimulations were delivered using transopercular electrodes exploring the parietal opercular cortex (SII area), the suprasylvian parietal cortex (SI area) and the insular cortex. SII responses were compared to those from adjacent SI and insular cortex. In the three areas we elicited mostly somatosensory responses, including paresthesiae, temperature and pain sensations. The rate of painful sensations (10%) was similar in SII and in the insula, while no painful sensation was evoked in SI. A few non-somatosensory responses were evoked by SII stimulation. Conversely various types of non-somatosensory responses (auditory, vegetative, vestibular, olfacto-gustatory, etc.) were evoked only by insular stimulation, confirming that SII, like SI, are mostly devoted to the processing of somatosensory inputs whereas the insular cortex is a polymodal area. We also found differences in size and lateralization of skin projection fields of evoked sensations between the three studied areas, showing a spatial resolution of the somatotopic map in SII intermediate between those found in SI and insula. This study shows the existence of three distinct somatosensory maps in the suprasylvian, opercular and insular regions, and separate pain representations in SII and insular cortex.

[1]  Mara Fabri,et al.  Cortical areas within the lateral sulcus connected to cutaneous representations in areas 3b and 1: A revised interpretation of the second somatosensory area in macaque monkeys , 1995, The Journal of comparative neurology.

[2]  R Kakigi,et al.  Topography of the secondary somatosensory cortex in humans: a magnetoencephalo-graphic study. , 1999, Neuroreport.

[3]  H. Burton,et al.  Somatic submodality distribution within the second somatosensory (SII), 7b, retroinsular, postauditory, and granular insular cortical areas of M. fascicularis , 1980, The Journal of comparative neurology.

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

[5]  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.

[6]  R. Hari,et al.  Functional Organization of the Human First and Second Somatosensory Cortices: a Neuromagnetic Study , 1993, The European journal of neuroscience.

[7]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[8]  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.

[9]  H. Jasper,et al.  Epilepsy and the functional anatomy of the human brain , 1985 .

[10]  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.

[11]  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.

[12]  R. Fisher,et al.  Parameters for direct cortical electrical stimulation in the human: histopathologic confirmation. , 1990, Electroencephalography and clinical neurophysiology.

[13]  M. Sur,et al.  Representations of the body surface in postcentral parietal cortex of Macaca fascicularis , 1980, The Journal of comparative neurology.

[14]  E. Disbrow,et al.  Brain processing of capsaicin-induced secondary hyperalgesia , 1999, Neurology.

[15]  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.

[16]  Harold Burton,et al.  Second Somatosensory Cortex and Related Areas , 1986 .

[17]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[18]  Alan C. Evans,et al.  Functional imaging of an illusion of pain , 1996, Nature.

[19]  Alan C. Evans,et al.  Distributed processing of pain and vibration by the human brain , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  P M Rossini,et al.  Topographic organization of the human primary and secondary somatosensory areas: an fMRI study , 2000, Neuroreport.

[21]  François Mauguière,et al.  Clinical Manifestations of Insular Lobe Seizures: A Stereo‐electroencephalographic Study , 2004 .

[22]  C. C. Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity. , 1989, Journal of neurophysiology.

[23]  T L Babb,et al.  A circuit for safe diagnostic electrical stimulation of the human brain. , 1980, Neurological research.

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

[25]  F Mauguière,et al.  Functional Mapping of the Insular Cortex: Clinical Implication in Temporal Lobe Epilepsy , 2000, Epilepsia.

[26]  M. Frot,et al.  Les réponses operculo-insulaires aux stimulations cutanées nociceptives chez l'homme. Revue de la littérature et données récentes , 1999, Neurophysiologie Clinique/Clinical Neurophysiology.

[27]  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.

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

[29]  D J Felleman,et al.  Somatotopic organization of the lateral sulcus of owl monkeys: Area 3b, s‐II, and a ventral somatosensory area , 1989, The Journal of comparative neurology.

[30]  R. Koeppe,et al.  Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain. , 1996, Journal of neurophysiology.

[31]  S F Miller,et al.  Burn size estimate reliability: a study. , 1991, The Journal of burn care & rehabilitation.

[32]  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 .

[33]  M. Honda,et al.  Pain-related somatosensory evoked potentials following CO2 laser stimulation of foot in man. , 1989, Electroencephalography and clinical neurophysiology.

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

[35]  V. Jousmäki,et al.  Activation of a distributed somatosensory cortical network in the human brain. A dipole modelling study of magnetic fields evoked by median nerve stimulation. Part I: Location and activation timing of SEF sources. , 1997, Electroencephalography and clinical neurophysiology.

[36]  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.

[37]  H. Dinse,et al.  Functional Imaging of Perceptual Learning in Human Primary and Secondary Somatosensory Cortex , 2003, Neuron.

[38]  Y. Lamour,et al.  Altered properties and laminar distribution of neuronal responses to peripheral stimulation in the Sml cortex of the arthritic rat , 1983, Brain Research.

[39]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[40]  W. Penfield,et al.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1968 .

[41]  R A Koeppe,et al.  Positron emission tomographic analysis of cerebral structures activated specifically by repetitive noxious heat stimuli. , 1994, Journal of neurophysiology.

[42]  R P Lesser,et al.  The second sensory area in humans: Evoked potential and electrical stimulation studies , 1985, Annals of neurology.

[43]  N. Thakor,et al.  Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. , 1993, Electroencephalography and clinical neurophysiology.

[44]  L Krubitzer,et al.  A redefinition of somatosensory areas in the lateral sulcus of macaque monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  J. Talairach,et al.  Stereotaxic Approach to Epilepsy , 1973 .

[46]  E. Adrian Afferent discharges to the cerebral cortex from peripheral sense organs , 1941, The Journal of physiology.

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

[48]  A. Vania Apkarian,et al.  Spinothalamocortical projections to the secondary somatosensory cortex (SII) in squirrel monkey , 1993, Brain Research.