Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations

We illustrate a general principal of electrical potential measurements from the surface of the cerebral cortex, by revisiting and reanalyzing experimental work from the visual, language and motor systems. A naive decomposition technique of electrocorticographic power spectral measurements reveals that broadband spectral changes reliably track task engagement. These broadband changes are shown to be a generic correlate of local cortical function across a variety of brain areas and behavioral tasks. Furthermore, they fit a power-law form that is consistent with simple models of the dendritic integration of asynchronous local population firing. Because broadband spectral changes covary with diverse perceptual and behavioral states on the timescale of 20-50 ms, they provide a powerful and widely applicable experimental tool.

[1]  G. Buzsáki,et al.  Cellular bases of hippocampal EEG in the behaving rat , 1983, Brain Research Reviews.

[2]  N. Mesgarani,et al.  Selective cortical representation of attended speaker in multi-talker speech perception , 2012, Nature.

[3]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[4]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[5]  W. Regehr,et al.  Timing of neurotransmission at fast synapses in the mammalian brain , 1996, Nature.

[6]  M. Steriade Grouping of brain rhythms in corticothalamic systems , 2006, Neuroscience.

[7]  Nick F. Ramsey,et al.  Detection of spontaneous class-specific visual stimuli with high temporal accuracy in human electrocorticography , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[8]  G. A. Woonton,et al.  EFFECTS OF ESERINE, ACETYLCHOLINE AND ATROPINE ON THE ELECTROCORTICOGRAM , 1940 .

[9]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[10]  Bijan Pesaran,et al.  Neural Correlates of Visual–Spatial Attention in Electrocorticographic Signals in Humans , 2011, Front. Hum. Neurosci..

[11]  N. Birbaumer,et al.  BCI2000: a general-purpose brain-computer interface (BCI) system , 2004, IEEE Transactions on Biomedical Engineering.

[12]  R. Irizarry,et al.  Electrocorticographic gamma activity during word production in spoken and sign language , 2001, Neurology.

[13]  Marc W Howard,et al.  Theta and Gamma Oscillations during Encoding Predict Subsequent Recall , 2003, The Journal of Neuroscience.

[14]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[15]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[16]  Richard L. Hughson,et al.  Extracting fractal components from time series , 1993 .

[17]  Rajesh P. N. Rao,et al.  Beyond the Gamma Band: The Role of High-Frequency Features in Movement Classification , 2008, IEEE Transactions on Biomedical Engineering.

[18]  Gert Pfurtscheller,et al.  EEG event-related desynchronization (ERD) and synchronization (ERS) , 1997 .

[19]  F. L. D. Silva,et al.  Event-Related Desynchronization , 1999 .

[20]  K. Miller Broadband Spectral Change: Evidence for a Macroscale Correlate of Population Firing Rate? , 2010, The Journal of Neuroscience.

[21]  Kai J Miller,et al.  Rapid online language mapping with electrocorticography. , 2011, Journal of neurosurgery. Pediatrics.

[22]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[23]  N. Logothetis,et al.  Frequency-Band Coupling in Surface EEG Reflects Spiking Activity in Monkey Visual Cortex , 2009, Neuron.

[24]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[25]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[26]  Gert Pfurtscheller,et al.  Functional meaning of event-related desynchronization (ERD) end synchronization (ERS) , 1999 .

[27]  E. Fetz,et al.  Decoupling the Cortical Power Spectrum Reveals Real-Time Representation of Individual Finger Movements in Humans , 2009, The Journal of Neuroscience.

[28]  Nick F. Ramsey,et al.  Automated electrocorticographic electrode localization on individually rendered brain surfaces , 2010, Journal of Neuroscience Methods.

[29]  Michael Okun,et al.  The Subthreshold Relation between Cortical Local Field Potential and Neuronal Firing Unveiled by Intracellular Recordings in Awake Rats , 2010, The Journal of Neuroscience.

[30]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[31]  H. L. Andrews,et al.  BRAIN POTENTIALS AND VOLUNTARY MUSCLE ACTIVITY IN MAN , 1938 .

[32]  Rajesh P. N. Rao,et al.  Cortical activity during motor execution, motor imagery, and imagery-based online feedback , 2010, Proceedings of the National Academy of Sciences.

[33]  Rajesh P. N. Rao,et al.  Dynamic Modulation of Local Population Activity by Rhythm Phase in Human Occipital Cortex During a Visual Search Task , 2010, Front. Hum. Neurosci..

[34]  N. Crone,et al.  Cortical γ responses: searching high and low. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[35]  C. Koch,et al.  A brief history of time (constants). , 1996, Cerebral cortex.

[36]  G. Ojemann,et al.  Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks , 1999, Clinical Neurophysiology.

[37]  Nancy Kopell,et al.  Slow and fast inhibition and an H-current interact to create a theta rhythm in a model of CA1 interneuron network. , 2005, Journal of neurophysiology.

[38]  David E. Sigeti,et al.  High-frequency power spectra for systems subject to noise. , 1987, Physical review. A, General physics.

[39]  G. Brindley,et al.  The electrical activity in the motor cortex that accompanies voluntary movement. , 1972, The Journal of physiology.

[40]  Robert T. Knight,et al.  Spatiotemporal imaging of cortical activation during verb generation and picture naming , 2010, NeuroImage.

[41]  K. Miller,et al.  Direct electrophysiological measurement of human default network areas , 2009, Proceedings of the National Academy of Sciences.

[42]  N. Barbaro,et al.  Spatiotemporal Dynamics of Word Processing in the Human Brain , 2007, Front. Neurosci..

[43]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[44]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

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

[46]  Juan R. Vidal,et al.  Category-Specific Visual Responses: An Intracranial Study Comparing Gamma, Beta, Alpha, and ERP Response Selectivity , 2010, Front. Hum. Neurosci..

[47]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[48]  G. Schalk,et al.  Decoding vowels and consonants in spoken and imagined words using electrocorticographic signals in humans , 2011, Journal of neural engineering.

[49]  Nick F. Ramsey,et al.  Human Motor Cortical Activity Is Selectively Phase-Entrained on Underlying Rhythms , 2012, PLoS Comput. Biol..

[50]  John O'Keefe,et al.  The cognitive map as a hippocampus , 1979, Behavioral and Brain Sciences.

[51]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  Mohammad Dastjerdi,et al.  Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing , 2012, Proceedings of the National Academy of Sciences.

[53]  Michael A. DiSano,et al.  Intracranial EEG Reveals a Time- and Frequency-Specific Role for the Right Inferior Frontal Gyrus and Primary Motor Cortex in Stopping Initiated Responses , 2009, The Journal of Neuroscience.

[54]  C. Bédard,et al.  Does the 1/f frequency scaling of brain signals reflect self-organized critical states? , 2006, Physical review letters.

[55]  Jeffrey G. Ojemann,et al.  Power-Law Scaling in the Brain Surface Electric Potential , 2009, PLoS Comput. Biol..

[56]  H. Jasper,et al.  Electrocorticograms in man: Effect of voluntary movement upon the electrical activity of the precentral gyrus , 1949 .

[57]  W PENFIELD,et al.  Mechanisms of voluntary movement. , 1954, Brain : a journal of neurology.

[58]  J. A. Bates,et al.  Electrical activity of the cortex accompanying movement , 1951, The Journal of physiology.

[59]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[60]  Hindiael Belchior,et al.  On High-Frequency Field Oscillations (>100 Hz) and the Spectral Leakage of Spiking Activity , 2013, The Journal of Neuroscience.

[61]  N. Ramsey,et al.  Neurophysiologic correlates of fMRI in human motor cortex , 2012, Human brain mapping.

[62]  M. Whittington,et al.  Gamma Oscillations Induced by Kainate Receptor Activation in the Entorhinal Cortex In Vitro , 2003, The Journal of Neuroscience.

[63]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[64]  Theodore H. Bullock,et al.  Periodicity in wide-band time series , 2002 .

[65]  H. Jasper,et al.  Electrical Activity of the Brain , 1941 .

[66]  Michael J. Kahana,et al.  Neural Representations of Individual Stimuli in Humans Revealed by Gamma-Band Electrocorticographic Activity , 2009, The Journal of Neuroscience.

[67]  N Kopell,et al.  Gap Junctions between Interneuron Dendrites Can Enhance Synchrony of Gamma Oscillations in Distributed Networks , 2001, The Journal of Neuroscience.

[68]  T. Sejnowski,et al.  Regulation of spike timing in visual cortical circuits , 2008, Nature Reviews Neuroscience.

[69]  V. Aggarwal,et al.  Coherency between spike and LFP activity in M1 during hand movements , 2009, 2009 4th International IEEE/EMBS Conference on Neural Engineering.