A parietal–frontal network studied by somatosensory oddball MEG responses, and its cross-modal consistency

Previous studies using functional magnetic resonance imaging (fMRI) and event-related potentials (ERPs) of the brain have found that a distributed parietal-frontal neuronal network is activated in normals during both auditory and visual oddball tasks. The common cortical regions in this network are inferior parietal lobule (IPL)/supramarginal gyrus (SMG), anterior cingulate cortex (ACC), and dorsolateral prefrontal cortex (DLPFC). It is not clear whether the same network is activated by oddball tasks during somatosensory stimulation. The present study addressed this question by testing healthy adults as they performed a novel median-nerve oddball paradigm while undergoing magnetoencephalography (MEG). An automated multiple dipole analysis technique, the Multi-Start Spatio-Temporal (MSST) algorithm, localized multiple neuronal generators, and identified their time-courses. IPL/SMG, ACC, and DLPFC were reliably localized in the MEG median-nerve oddball responses, with IPL/SMG activation significantly preceding ACC and DLPFC activation. Thus, the same parietal-frontal neuronal network that shows activation during auditory and visual oddball tests is activated in a median-nerve oddball paradigm. Regions uniquely related to somatosensory oddball responses (e.g., primary and secondary somatosensory, dorsal premotor, primary motor, and supplementary motor areas) were also localized. Since the parietal-frontal network supports attentional allocation during performance of the task, this study may provide a novel method, as well as normative baseline data, for examining attention-related deficits in the somatosensory system of patients with neurological or psychiatric disorders.

[1]  What can we learn from MEG studies of the somatosensory system of the swine? , 1996, Electroencephalography and clinical neurophysiology. Supplement.

[2]  C. C. Wood,et al.  Cortical somatosensory evoked potentials. II. Effects of excision of somatosensory or motor cortex in humans and monkeys. , 1991, Journal of neurophysiology.

[3]  K. Kiehl,et al.  An event-related functional magnetic resonance imaging study of an auditory oddball task in schizophrenia , 2001, Schizophrenia Research.

[4]  F. H. Lopes da Silva,et al.  On the magnetic field distribution generated by a dipolar current source situated in a realistically shaped compartment model of the head. , 1987, Electroencephalography and clinical neurophysiology.

[5]  T. Yoshimoto,et al.  Neuromagnetic evidence of pre- and post-central cortical sources of somatosensory evoked responses. , 1996, Electroencephalography and clinical neurophysiology.

[6]  M. Weisend,et al.  Magnetoencephalographic characterization of sleep spindles in humans. , 1997, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[7]  S. Baumann,et al.  Late magnetic fields and positive evoked potentials following infrequent and unpredictable omissions of visual stimuli. , 1992, Electroencephalography and clinical neurophysiology.

[8]  M. Hämäläinen,et al.  Realistic conductivity geometry model of the human head for interpretation of neuromagnetic data , 1989, IEEE Transactions on Biomedical Engineering.

[9]  Veikko Jousmäki,et al.  Sensorimotor integration in human primary and secondary somatosensory cortices , 1998, Brain Research.

[10]  B. Turetsky,et al.  P300 subcomponent abnormalities in schizophrenia: I. Physiological evidence for gender and subtype specific differences in regional pathology , 1998, Biological Psychiatry.

[11]  B. J. Casey,et al.  Activation of the prefrontal cortex in a nonspatial working memory task with functional MRI , 1994, Human brain mapping.

[12]  Stephen J. Jones,et al.  Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings. , 1991, Brain : a journal of neurology.

[13]  Hiroshi Shibasaki,et al.  Attention modulates both primary and second somatosensory cortical activities in humans: a magnetoencephalographic study. , 1998, Journal of neurophysiology.

[14]  P. Goldman-Rakic,et al.  Infrequent events transiently activate human prefrontal and parietal cortex as measured by functional MRI. , 1997, Journal of neurophysiology.

[15]  J. Stephen,et al.  Sources on the anterior and posterior banks of the central sulcus identified from magnetic somatosensory evoked responses using Multi‐Start Spatio‐Temporal localization , 2000, Human brain mapping.

[16]  F Mauguière,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 II: Effects of stimulus rate, attention and stimulus detection. , 1997, Electroencephalography and clinical neurophysiology.

[17]  H. Yumiya,et al.  Peripheral input pathways to the monkey motor cortex , 1980, Experimental Brain Research.

[18]  A. S. Ferguson,et al.  A complete linear discretization for calculating the magnetic field using the boundary element method , 1994, IEEE Transactions on Biomedical Engineering.

[19]  J. Gawehn,et al.  Functional MRI of human primary somatosensory and motor cortex during median nerve stimulation , 1999, Clinical Neurophysiology.

[20]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[21]  M. Milham,et al.  Competition for priority in processing increases prefrontal cortex's involvement in top-down control: an event-related fMRI study of the stroop task. , 2003, Brain research. Cognitive brain research.

[22]  N Forss,et al.  Effects of stimulus intensity on signals from human somatosensory cortices , 1998, Neuroreport.

[23]  J. D. Munck The estimation of time varying dipoles on the basis of evoked potentials. , 1990 .

[24]  Ulrich Hegerl,et al.  Dipole source analysis of P300 component of the auditory evoked potential: a methodological advance? , 1997, Psychiatry Research: Neuroimaging.

[25]  R. Lemon Functional properties of monkey motor cortex neurones receiving afferent input from the hand and fingers , 1981, The Journal of physiology.

[26]  C Tomberg,et al.  Mapping early somatosensory evoked potentials in selective attention: critical evaluation of control conditions used for titrating by difference the cognitive P30, P40, P100 and N140. , 1989, Electroencephalography and clinical neurophysiology.

[27]  R. N. Lemon,et al.  Short-latency peripheral inputs to thalamic neurones projecting to the motor cortex in the monkey , 1979, Experimental Brain Research.

[28]  Samuel J. Williamson,et al.  Advances in Biomagnetism , 1990, Springer US.

[29]  R. Knight,et al.  Contributions of temporal-parietal junction to the human auditory P3 , 1989, Brain Research.

[30]  C J Hodge,et al.  Functional magnetic resonance imaging of somatosensory cortex activity produced by electrical stimulation of the median nerve or tactile stimulation of the index finger. , 2000, Journal of neurosurgery.

[31]  M. Shenton,et al.  Electrical source analysis of auditory ERPs in medial temporal lobe amnestic syndrome. , 1993, Electroencephalography and clinical neurophysiology.

[32]  B. Ardekani,et al.  Functional magnetic resonance imaging of brain activity in the visual oddball task. , 2002, Brain research. Cognitive brain research.

[33]  R. Hari,et al.  Phase locking between human primary and secondary somatosensory cortices , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[34]  P. S. Lewis,et al.  Monte Carlo Analysis of Localization Errors in Magnetoencephalography , 1989 .

[35]  John A. Nelder,et al.  A Simplex Method for Function Minimization , 1965, Comput. J..

[36]  F. Mauguière,et al.  Somatosensory responses during selective spatial attention: The N120‐to‐N140 trasition , 1995 .

[37]  J Régis,et al.  Short-latency components of evoked potentials to median nerve stimulation recorded by intracerebral electrodes in the human pre- and postcentral areas , 2004, Clinical Neurophysiology.

[38]  K. Sekihara,et al.  Noise covariance incorporated MEG-MUSIC algorithm: a method for multiple-dipole estimation tolerant of the influence of background brain activity , 1997, IEEE Transactions on Biomedical Engineering.

[39]  R. Hari,et al.  Separate finger representations at the human second somatosensory cortex , 1990, Neuroscience.

[40]  E. Halgren,et al.  Generators of the late cognitive potentials in auditory and visual oddball tasks. , 1998, Electroencephalography and clinical neurophysiology.

[41]  R. Porter,et al.  Afferent input to movement-related precentral neurones in conscious monkeys , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[42]  E. G. Jones,et al.  Differential thalamic relationships of sensory‐motor and parietal cortical fields in monkeys , 1979, The Journal of comparative neurology.

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

[44]  E. Halgren,et al.  The intracranial topography of the P3 event-related potential elicited during auditory oddball. , 1990, Electroencephalography and clinical neurophysiology.

[45]  Hiroshi Shibasaki,et al.  Second somatosensory area (SII) plays a significant role in selective somatosensory attention. , 2002, Brain research. Cognitive brain research.

[46]  R. Benson,et al.  Responses to rare visual target and distractor stimuli using event-related fMRI. , 2000, Journal of neurophysiology.

[47]  Roland R. Lee,et al.  Temporal dynamics of ipsilateral and contralateral motor activity during voluntary finger movement , 2004, Human brain mapping.

[48]  J. Rohrbaugh,et al.  Endogenous potentials generated in the human hippocampal formation and amygdala by infrequent events. , 1980, Science.

[49]  J. Stephen,et al.  Central versus peripheral visual field stimulation results in timing differences in dorsal stream sources as measured with MEG , 2002, Vision Research.

[50]  R M Leahy,et al.  A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. , 1999, Physics in medicine and biology.

[51]  R. A. Davidoff The pyramidal tract. , 1990, Neurology.

[52]  R. Hari,et al.  Activation of the human posterior parietal cortex by median nerve stimulation , 2004, Experimental Brain Research.

[53]  P. Skudlarski,et al.  Event-related fMRI of auditory and visual oddball tasks. , 2000, Magnetic resonance imaging.

[54]  L. Heller,et al.  Evaluation of boundary element methods for the EEG forward problem: effect of linear interpolation , 1995, IEEE Transactions on Biomedical Engineering.

[55]  T. R. Knösche,et al.  Determining the Number of Independent Sources of the EEG: A Simulation Study on Information Criteria , 2004, Brain Topography.

[56]  E Halgren,et al.  Endogenous potentials evoked in simple cognitive tasks: depth components and task correlates. , 1987, Electroencephalography and clinical neurophysiology.

[57]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[58]  M. Merzenich,et al.  Reorganization of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. , 1987, Progress in brain research.

[59]  F. Plum Handbook of Physiology. , 1960 .

[60]  S. Hillyard,et al.  Similarities and differences among the P3 waves to detected signals in three modalities. , 1980, Psychophysiology.

[61]  R D Pascual-Marqui,et al.  Differential effects of normal aging on sources of standard N1, target N1 and target P300 auditory event-related brain potentials revealed by low resolution electromagnetic tomography (LORETA). , 1998, Electroencephalography and clinical neurophysiology.

[62]  Hiroshi Miyazato,et al.  Abnormalities of auditory P300 cortical current density in patients with schizophrenia using high density recording. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[63]  M Huang,et al.  Multi-start downhill simplex method for spatio-temporal source localization in magnetoencephalography. , 1998, Electroencephalography and clinical neurophysiology.

[64]  H. Asanuma,et al.  Peripheral afferent inputs to the forelimb area of the monkey motor cortex: Input-output relations , 2004, Experimental Brain Research.

[65]  P. Goldman-Rakic,et al.  Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. , 1996, Cerebral cortex.

[66]  G L Romani,et al.  Tonotopic organization of the human auditory cortex revealed by steady state neuromagnetic measurements. , 1986, Acta oto-laryngologica. Supplementum.

[67]  Karl J. Friston,et al.  Incorporating Prior Knowledge into Image Registration , 1997, NeuroImage.

[68]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[69]  M. E. Spencer,et al.  A Study of Dipole Localization Accuracy for MEG and EEG using a Human Skull Phantom , 1998, NeuroImage.

[70]  F. Baldissera,et al.  Afferent excitation of human motor cortex as revealed by enhancement of direct cortico-spinal actions on motoneurones. , 1995, Electroencephalography and clinical neurophysiology.

[71]  R. Knight,et al.  P300 generation by novel somatosensory stimuli. , 1991, Electroencephalography and clinical neurophysiology.

[72]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[73]  B. Turetsky,et al.  P300 Subcomponent Abnormalities in Schizophrenia: Longitudinal Stability and Relationship to Symptom Change , 1998, Biological Psychiatry.

[74]  C C Wood,et al.  Intracranial recordings of endogenous ERPs in humans. , 1985, Electroencephalography and clinical neurophysiology. Supplement.

[75]  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.

[76]  H. Lüders,et al.  Recording of event-related potentials (P300) from human cortex. , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[77]  Alec Marantz,et al.  MEG spatio-temporal analysis using a covariance matrix calculated from nonaveraged multiple-epoch data , 1999 .

[78]  E Donchin,et al.  A cortical potential imaging analysis of the P300 and Novelty P3 components , 2001, Human brain mapping.

[79]  A Urbano,et al.  Human short latency cortical responses to somatosensory stimulation. A high resolution EEG study , 1997, Neuroreport.

[80]  T. Yoshiura,et al.  Functional MRI study of auditory and visual oddball tasks. , 1999, Neuroreport.

[81]  Edward Awh,et al.  Spatial versus Object Working Memory: PET Investigations , 1995, Journal of Cognitive Neuroscience.

[82]  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.

[83]  E. G. Jones,et al.  Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys , 1978, The Journal of comparative neurology.

[84]  R. Goebel,et al.  The functional neuroanatomy of target detection: an fMRI study of visual and auditory oddball tasks. , 1999, Cerebral cortex.

[85]  C. Aine,et al.  Multistart Algorithms for MEG Empirical Data Analysis Reliably Characterize Locations and Time Courses of Multiple Sources , 2000, NeuroImage.

[86]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. , 1995, Electroencephalography and clinical neurophysiology.

[87]  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 .

[88]  R. Hari,et al.  Magnetoencephalography in the study of human somatosensory cortical processing. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[89]  P. Goldman-Rakic,et al.  Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[90]  Mingxiong Huang,et al.  A non-invasive method for observing hippocampal function , 2003, Neuroreport.

[91]  R. Ilmoniemi,et al.  Somatosensory evoked magnetic fields to median nerve stimulation: interhemispheric differences in a normal population. , 1997, Electroencephalography and clinical neurophysiology.

[92]  J. Ford,et al.  Combined event‐related fMRI and EEG evidence for temporal—parietal cortex activation during target detection , 1997, Neuroreport.

[93]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[94]  Akitake Kanno,et al.  Ipsilateral Area 3b Responses to Median Nerve Somatosensory Stimulation , 2003, NeuroImage.

[95]  H. Vaughan,et al.  Topographic analysis of auditory event-related potentials associated with acoustic and semantic processing. , 1988, Electroencephalography and clinical neurophysiology.

[96]  I. Kiss,et al.  A parieto-occipital generator for P300: evidence from human intracranial recordings. , 1989, The International journal of neuroscience.

[97]  Peter Teale,et al.  Anomalous somatosensory cortical localization in schizophrenia. , 2003, The American journal of psychiatry.

[98]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[99]  A. Papanicolaou,et al.  Electric source localization of the auditory P300 agrees with magnetic source localization. , 1995, Electroencephalography and clinical neurophysiology.

[100]  W. Ritter,et al.  The scalp topography of potentials associated with missing visual or auditory stimuli. , 1976, Electroencephalography and clinical neurophysiology.

[101]  D. Harrington,et al.  MEG response to median nerve stimulation correlates with recovery of sensory and motor function after stroke , 2004, Clinical Neurophysiology.

[102]  Julia M Stephen,et al.  Investigation of the normal proximal somatomotor system using magnetoencephalography , 2003, Clinical Neurophysiology.

[103]  C C Wood,et al.  Electrical sources in human somatosensory cortex: identification by combined magnetic and potential recordings. , 1985, Science.

[104]  J. Murphy,et al.  Spatial organization of precentral cortex in awake primates. I. Somatosensory inputs. , 1978, Journal of neurophysiology.

[105]  P. Goldman-Rakic Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[106]  P. Fedio,et al.  Task-related changes in P300 scalp distribution in temporal lobectomy patients. , 1987, Electroencephalography and clinical neurophysiology. Supplement.

[107]  J. Sarvas Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[108]  C. Yingling,et al.  A subcortical correlate of P300 in man. , 1984, Electroencephalography and clinical neurophysiology.

[109]  Gene H. Golub,et al.  Matrix computations , 1983 .

[110]  H Hämäläinen,et al.  Is the somatosensory N250 related to deviance discrimination or conscious target detection? , 1996, Electroencephalography and clinical neurophysiology.

[111]  François Mauguière,et al.  Stereotactic recordings of median nerve somatosensory‐evoked potentials in the human pre‐supplementary motor area , 2001, The European journal of neuroscience.