The relationship between magnetic and electrophysiological responses to complex tactile stimuli

BackgroundMagnetoencephalography (MEG) has become an increasingly popular technique for non-invasively characterizing neuromagnetic field changes in the brain at a high temporal resolution. To examine the reliability of the MEG signal, we compared magnetic and electrophysiological responses to complex natural stimuli from the same animals. We examined changes in neuromagnetic fields, local field potentials (LFP) and multi-unit activity (MUA) in macaque monkey primary somatosensory cortex that were induced by varying the rate of mechanical stimulation. Stimuli were applied to the fingertips with three inter-stimulus intervals (ISIs): 0.33s, 1s and 2s.ResultsSignal intensity was inversely related to the rate of stimulation, but to different degrees for each measurement method. The decrease in response at higher stimulation rates was significantly greater for MUA than LFP and MEG data, while no significant difference was observed between LFP and MEG recordings. Furthermore, response latency was the shortest for MUA and the longest for MEG data.ConclusionThe MEG signal is an accurate representation of electrophysiological responses to complex natural stimuli. Further, the intensity and latency of the MEG signal were better correlated with the LFP than MUA data suggesting that the MEG signal reflects primarily synaptic currents rather than spiking activity. These differences in latency could be attributed to differences in the extent of spatial summation and/or differential laminar sensitivity.

[1]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[2]  D. Kleinfeld,et al.  Adaptive Filtering of Vibrissa Input in Motor Cortex of Rat , 2002, Neuron.

[3]  William Sutherling,et al.  Intracellular currents of interictal penicillin spikes: Evidence from neuromagnetic mapping , 1986, Brain Research.

[4]  M. Castro-Alamancos,et al.  Absence of Rapid Sensory Adaptation in Neocortex during Information Processing States , 2004, Neuron.

[5]  Y. Okada,et al.  Synchronized spikes of thalamocortical axonal terminals and cortical neurons are detectable outside the pig brain with MEG. , 2002, Journal of neurophysiology.

[6]  Greg C. Champney,et al.  Rate code and temporal code for frequency of whisker stimulation in rat primary and secondary somatic sensory cortex , 2006, Experimental Brain Research.

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

[8]  E. Disbrow,et al.  Activation of the somatosensory cortex during Aβ-fiber mediated hyperalgesia a MSI study , 2000, Brain Research.

[9]  N. Logothetis.  The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal , 2003, The Journal of Neuroscience.

[10]  Afonso C. Silva,et al.  Laminar specificity of functional MRI onset times during somatosensory stimulation in rat , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Adrian T. Lee,et al.  Discrimination of Large Venous Vessels in Time‐Course Spiral Blood‐Oxygen‐Level‐Dependent Magnetic‐Resonance Functional Neuroimaging , 1995, Magnetic resonance in medicine.

[12]  D. Cohen.  Magnetoencephalography: Detection of the Brain's Electrical Activity with a Superconducting Magnetometer , 1972, Science.

[13]  E C Wong,et al.  Processing strategies for time‐course data sets in functional mri of the human brain , 1993, Magnetic resonance in medicine.

[14]  N. Logothetis.  The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[15]  H Pratt,et al.  Mechanically and electrically evoked somatosensory potentials in humans: effects of stimulus presentation rate. , 1980, Electroencephalography and clinical neurophysiology.

[16]  D J Simons,et al.  Adaptation in thalamic barreloid and cortical barrel neurons to periodic whisker deflections varying in frequency and velocity. , 2004, Journal of neurophysiology.

[17]  Y. Okada,et al.  Physiological origins of evoked magnetic fields and extracellular field potentials produced by guinea‐pig CA3 hippocampal slices , 2002, The Journal of physiology.

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

[19]  Charles Nicholson,et al.  Magnetic field associated with spreading depression: a model for the detection of migraine , 1988, Brain Research.

[20]  M. Lauritzen,et al.  Relationship of Spikes, Synaptic Activity, and Local Changes of Cerebral Blood Flow , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[21]  Klas H. Pettersen,et al.  Laminar population analysis: estimating firing rates and evoked synaptic activity from multielectrode recordings in rat barrel cortex. , 2007, Journal of neurophysiology.

[22]  C. Nicholson,et al.  MEG source models and physiology. , 1987, Physics in medicine and biology.

[23]  G Curio,et al.  Localization of evoked neuromagnetic 600 Hz activity in the cerebral somatosensory system. , 1994, Electroencephalography and clinical neurophysiology.

[24]  C C Wood,et al.  Cortical somatosensory evoked potentials. I. Recordings in the monkey Macaca fascicularis. , 1991, Journal of neurophysiology.

[25]  E A Disbrow,et al.  Quantification and reproducibility of tracking cortical extent of activation by use of functional MR imaging and magnetoencephalography. , 2000, AJNR. American journal of neuroradiology.

[26]  Y. Okada,et al.  Genesis of MEG signals in a mammalian CNS structure. , 1997, Electroencephalography and clinical neurophysiology.

[27]  B. Connors,et al.  Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. , 1999, Journal of neurophysiology.

[28]  A Schnitzler,et al.  Different cortical organization of visceral and somatic sensation in humans , 1999, The European journal of neuroscience.

[29]  D. Barth,et al.  The electrophysiological basis of epileptiform magnetic fields in neocortex: spontaneous ictal phenomena , 1991, Brain Research.

[30]  J. Rajapakse,et al.  Human Brain Mapping 6:283–300(1998) � Modeling Hemodynamic Response for Analysis of Functional MRI Time-Series , 2022 .

[31]  T Imada,et al.  Somatic evoked high-frequency magnetic oscillations reflect activity of inhibitory interneurons in the human somatosensory cortex. , 1996, Electroencephalography and clinical neurophysiology.

[32]  William Sutherling,et al.  Current source-density and neuromagnetic analysis of the direct cortical response in rat cortex , 1988, Brain Research.

[33]  A. Ngai,et al.  Frequency-dependent changes in cerebral blood flow and evoked potentials during somatosensory stimulation in the rat , 1999, Brain Research.

[34]  Y. Okada,et al.  Origins of the somatic N20 and high-frequency oscillations evoked by trigeminal stimulation in the piglets , 2005, Clinical Neurophysiology.

[35]  C. Nicholson,et al.  Multimodal characterization of population responses evoked by applied electric field in vitro: extracellular potential, magnetic evoked field, transmembrane potential, and current-source density analysis , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  J Beatty,et al.  Fast and slow magnetic phenomena in focal epileptic seizures. , 1984, Science.

[37]  K. Hossmann,et al.  Simultaneous recording of evoked potentials and T  *2 ‐weighted MR images during somatosensory stimulation of rat , 1999, Magnetic resonance in medicine.

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

[39]  U. Mitzdorf.  Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[40]  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.

[41]  J. Mäkelä,et al.  Serial processing of the somesthetic information revealed by different effects of stimulus rate on the somatosensory-evoked potentials and magnetic fields , 1998, Brain Research.

[42]  D. Noll,et al.  Nonlinear Aspects of the BOLD Response in Functional MRI , 1998, NeuroImage.

[43]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

[44]  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.

[45]  Bernd Lütkenhöner,et al.  Efficient neuromagnetic determination of landmarks in the somatosensory cortex , 2000, Clinical Neurophysiology.

[46]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[47]  Cpj de Kock,et al.  Layer‐ and cell‐type‐specific suprathreshold stimulus representation in rat primary somatosensory cortex , 2007, The Journal of physiology.

[48]  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.

[49]  D. Simons.  Response properties of vibrissa units in rat SI somatosensory neocortex. , 1978, Journal of neurophysiology.

[50]  John E. W. Mayhew,et al.  Investigating neural–hemodynamic coupling and the hemodynamic response function in the awake rat , 2006, NeuroImage.

[51]  Srikantan S Nagarajan,et al.  Spatiotemporal integration of tactile information in human somatosensory cortex , 2007, BMC Neuroscience.

[52]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.

[53]  R Salmelin,et al.  Comparison of somatosensory evoked fields to airpuff and electric stimuli. , 1994, Electroencephalography and clinical neurophysiology.

[54]  R. R. Sturrock,et al.  Problems of the Keimbahn: New Work on Mammalian Germ Cell Lineage , 1985 .

[55]  Ned Jenkinson,et al.  Stimulus Frequency Processing in Awake Rat Barrel Cortex , 2006, The Journal of Neuroscience.

[56]  Richard M. Leahy,et al.  Electromagnetic brain mapping , 2001, IEEE Signal Process. Mag..

[57]  M Bach,et al.  Coupling of neural activity and BOLD fMRI response: New insights by combination of fMRI and VEP experiments in transition from single events to continuous stimulation , 2001, Magnetic resonance in medicine.

[58]  Christoph Stippich,et al.  Interaction of Tactile Input in the Human Primary and Secondary Somatosensory Cortex—A Magnetoencephalographic Study , 2001, NeuroImage.

[59]  Uzay E. Emir,et al.  Changes in BOLD transients with visual stimuli across 1–44Hz , 2008, Neuroscience Letters.

[60]  S. Nelson,et al.  Short-Term Depression at Thalamocortical Synapses Contributes to Rapid Adaptation of Cortical Sensory Responses In Vivo , 2002, Neuron.

[61]  John E. W. Mayhew,et al.  The effect of hypercapnia on the neural and hemodynamic responses to somatosensory stimulation , 2005, NeuroImage.

[62]  Y. Okada,et al.  Detection of magnetic evoked fields associated with synchronous population activities in the transverse CA1 slice of the guinea pig. , 1993, Journal of neurophysiology.

[63]  Dominique L. Pritchett,et al.  Neural Correlates of Tactile Detection: A Combined Magnetoencephalography and Biophysically Based Computational Modeling Study , 2007, The Journal of Neuroscience.

[64]  Y. Okada,et al.  Contributions of principal neocortical neurons to magnetoencephalography and electroencephalography signals , 2006, The Journal of physiology.

[65]  R. Ilmoniemi,et al.  Effects of interstimulus interval on somatosensory evoked magnetic fields (SEFs): a hypothesis concerning SEF generation at the primary sensorimotor cortex. , 1996, Electroencephalography and clinical neurophysiology.

[66]  C. Nicholson,et al.  Theoretical analysis of field potentials in anisotropic ensembles of neuronal elements. , 1973, IEEE transactions on bio-medical engineering.

[67]  Anders Dale,et al.  Band-pass response properties of rat SI neurons. , 2003, Journal of neurophysiology.

[68]  A. P. Bannister,et al.  Inter- and intra-laminar connections of pyramidal cells in the neocortex , 2005, Neuroscience Research.

[69]  E Ahissar,et al.  Temporal frequency of whisker movement. II. Laminar organization of cortical representations. , 2001, Journal of neurophysiology.

[70]  K. Reinikainen,et al.  Rate effect and mismatch responses in the somatosensory system: ERP-recordings in humans , 1997, Biological Psychology.

[71]  H. Vaughan,et al.  Topography and intracranial sources of somatosensory evoked potentials in the monkey. II. Cortical components. , 1981, Electroencephalography and clinical neurophysiology.

[72]  Erika E. Fanselow,et al.  Behavioral Modulation of Tactile Responses in the Rat Somatosensory System , 1999, The Journal of Neuroscience.

[73]  Y. Okada,et al.  Physiological bases of the synchronized population spikes and slow wave of the magnetic field generated by a guinea-pig longitudinal CA3 slice preparation. , 1998, Electroencephalography and clinical neurophysiology.

[74]  E. Disbrow,et al.  Activation of the somatosensory cortex during Aβ-fiber mediated hyperalgesia - a MSI study , 2000, NeuroImage.

[75]  Y. Okada,et al.  Contribution of Ionic Currents to Magnetoencephalography (MEG) and Electroencephalography (EEG) Signals Generated by Guinea‐Pig CA3 Slices , 2003, The Journal of physiology.

[76]  M Hämäläinen,et al.  Early deflections of cerebral magnetic responses to median nerve stimulation. , 1989, Electroencephalography and clinical neurophysiology.

[77]  C. Nicholson,et al.  Magnetic evoked field associated with transcortical currents in turtle cerebellum. , 1988, Biophysical journal.

[78]  L. Krubitzer,et al.  Evidence for interhemispheric processing of inputs from the hands in human S2 and PV. , 2001, Journal of neurophysiology.

[79]  E P Gardner,et al.  Somatosensory evoked potentials (SEPs) and cortical single unit responses elicited by mechanical tactile stimuli in awake monkeys. , 1984, Electroencephalography and clinical neurophysiology.

[80]  Mriganka Sur,et al.  Somatosensory cortex in macaque monkeys: laminar differences in receptive field size in areas 3b and 1 , 1985, Brain Research.

[81]  D. Contreras,et al.  Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation , 2006, The Journal of Neuroscience.

[82]  Magnetic field associated with neural activities in an isolated cerebellum , 1987, Brain Research.

[83]  M. Armstrong‐James,et al.  Flow of excitation within rat barrel cortex on striking a single vibrissa. , 1992, Journal of neurophysiology.