The Spatial Reach of Neuronal Coherence and Spike-Field Coupling across the Human Neocortex. 2022

John C Myers, and Elliot H Smith, and Marcin Leszczynski, and James O'Sullivan, and Mark J Yates, and Guy McKhann, and Nima Mesgarani, and Charles Schroeder, and Catherine Schevon, and Sameer A Sheth
Department of Neurosurgery, Baylor College of Medicine, Houston, Texas 77030 john.myers@bcm.edu.

Neuronal coherence is thought to be a fundamental mechanism of communication in the brain, where synchronized field potentials coordinate synaptic and spiking events to support plasticity and learning. Although the spread of field potentials has garnered great interest, little is known about the spatial reach of phase synchronization, or neuronal coherence. Functional connectivity between different brain regions is known to occur across long distances, but the locality of synchronization across the neocortex is understudied. Here we used simultaneous recordings from electrocorticography (ECoG) grids and high-density microelectrode arrays to estimate the spatial reach of neuronal coherence and spike-field coherence (SFC) across frontal, temporal, and occipital cortices during cognitive tasks in humans. We observed the strongest coherence within a 2-3 cm distance from the microelectrode arrays, potentially defining an effective range for local communication. This range was relatively consistent across brain regions, spectral frequencies, and cognitive tasks. The magnitude of coherence showed power law decay with increasing distance from the microelectrode arrays, where the highest coherence occurred between ECoG contacts, followed by coherence between ECoG and deep cortical local field potential (LFP), and then SFC (i.e., ECoG > LFP > SFC). The spectral frequency of coherence also affected its magnitude. Alpha coherence (8-14 Hz) was generally higher than other frequencies for signals nearest the microelectrode arrays, whereas delta coherence (1-3 Hz) was higher for signals that were farther away. Action potentials in all brain regions were most coherent with the phase of alpha oscillations, which suggests that alpha waves could play a larger, more spatially local role in spike timing than other frequencies. These findings provide a deeper understanding of the spatial and spectral dynamics of neuronal synchronization, further advancing knowledge about how activity propagates across the human brain.SIGNIFICANCE STATEMENT Coherence is theorized to facilitate information transfer across cerebral space by providing a convenient electrophysiological mechanism to modulate membrane potentials in spatiotemporally complex patterns. Our work uses a multiscale approach to evaluate the spatial reach of phase coherence and spike-field coherence during cognitive tasks in humans. Locally, coherence can reach up to 3 cm around a given area of neocortex. The spectral properties of coherence revealed that alpha phase-field and spike-field coherence were higher within ranges <2 cm, whereas lower-frequency delta coherence was higher for contacts farther away. Spatiotemporally shared information (i.e., coherence) across neocortex seems to reach farther than field potentials alone.

UI MeSH Term Description Entries
D008839 Microelectrodes Electrodes with an extremely small tip, used in a voltage clamp or other apparatus to stimulate or record bioelectric potentials of single cells intracellularly or extracellularly. (Dorland, 28th ed) Electrodes, Miniaturized,Electrode, Miniaturized,Microelectrode,Miniaturized Electrode,Miniaturized Electrodes
D009474 Neurons The basic cellular units of nervous tissue. Each neuron consists of a body, an axon, and dendrites. Their purpose is to receive, conduct, and transmit impulses in the NERVOUS SYSTEM. Nerve Cells,Cell, Nerve,Cells, Nerve,Nerve Cell,Neuron
D006801 Humans Members of the species Homo sapiens. Homo sapiens,Man (Taxonomy),Human,Man, Modern,Modern Man
D000069280 Electrocorticography Recording of brain electrical activities in which the electrodes are placed directly on the CEREBRAL CORTEX. Electrocorticography (EcoG),Extraoperative ECoG,Extraoperative Electrocorticography,Intracranial EEG,Intracranial Electroencephalography,Intraoperative ECoG,Intraoperative Electrocorticography,ECoG, Extraoperative,ECoG, Intraoperative,ECoGs, Extraoperative,ECoGs, Intraoperative,EEG, Intracranial,EEGs, Intracranial,Electrocorticographies,Electrocorticographies (EcoG),Electrocorticographies, Extraoperative,Electrocorticographies, Intraoperative,Electrocorticography, Extraoperative,Electrocorticography, Intraoperative,Electroencephalographies, Intracranial,Electroencephalography, Intracranial,Extraoperative ECoGs,Extraoperative Electrocorticographies,Intracranial EEGs,Intracranial Electroencephalographies,Intraoperative ECoGs,Intraoperative Electrocorticographies
D000200 Action Potentials Abrupt changes in the membrane potential that sweep along the CELL MEMBRANE of excitable cells in response to excitation stimuli. Spike Potentials,Nerve Impulses,Action Potential,Impulse, Nerve,Impulses, Nerve,Nerve Impulse,Potential, Action,Potential, Spike,Potentials, Action,Potentials, Spike,Spike Potential
D019579 Neocortex The largest portion of the CEREBRAL CORTEX in which the NEURONS are arranged in six layers in the mammalian brain: molecular, external granular, external pyramidal, internal granular, internal pyramidal and multiform layers. Cerebral Neocortex,External Granular Layer,Isocortex,Neocortical External Granular Layer,Neocortical External Pyramidal Layer,Neocortical Internal Granular Layer,Neocortical Internal Pyramidal Layer,Neocortical Molecular Layer,Neocortical Multiform Layer,Neopallial Cortex,Neopallium,Substantia Corticalis,Cerebral Neocortices,Cortex, Neopallial,Corticali, Substantia,Corticalis, Substantia,Cortices, Neopallial,External Granular Layers,Granular Layer, External,Granular Layers, External,Isocortices,Layer, External Granular,Layer, Neocortical Molecular,Layer, Neocortical Multiform,Layers, External Granular,Layers, Neocortical Molecular,Layers, Neocortical Multiform,Molecular Layer, Neocortical,Molecular Layers, Neocortical,Multiform Layer, Neocortical,Multiform Layers, Neocortical,Neocortex, Cerebral,Neocortical Molecular Layers,Neocortical Multiform Layers,Neocortices,Neocortices, Cerebral,Neopallial Cortices,Neopalliums,Substantia Corticali

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