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The Origin of Extracellular Fields and Currents — EEG, Ecog, LFP and Spikes

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The Origin of Extracellular Fields and Currents — EEG, Ecog, LFP and Spikes REVIEWS The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes György Buzsáki1,2,3, Costas A. Anastassiou4 and Christof Koch4,5 Abstract | Neuronal activity in the brain gives rise to transmembrane currents that can be measured in the extracellular medium. Although the major contributor of the extracellular signal is the synaptic transmembrane current, other sources — including Na+ and Ca2+ spikes, ionic fluxes through voltage- and ligand-gated channels, and intrinsic membrane oscillations — can substantially shape the extracellular field. High-density recordings of field activity in animals and subdural grid recordings in humans, combined with recently developed data processing tools and computational modelling, can provide insight into the cooperative behaviour of neurons, their average synaptic input and their spiking output, and can increase our understanding of how these processes contribute to the extracellular signal. Electric current contributions from all active cellular Recent advances in microelectrode technology processes within a volume of brain tissue superimpose using silicon-based polytrodes offer new possibilities at a given location in the extracellular medium and for estimating input–output transfer functions in vivo, generate a potential, Ve (a scalar measured in Volts), and high-density recordings of electric and magnetic with respect to a reference potential. The difference in fields of the brain now provide unprecedented spatial Ve between two locations gives rise to an electric field coverage and resolution of the elementary processes (a vector whose amplitude is measured in Volts per involved in generating the extracellular field. In 1Center for Molecular and distance) that is defined as the negative spatial gradient addition, novel time-resolved spectral methods provide Behavioural Neuroscience, of Ve. Electric fields can be monitored by extracellularly insights into the functional meaning of the information- Rutgers, The State University placed electrodes with submillisecond time resolution rich high-frequency bands of the V signal3,4. These of New Jersey, e 197 University Avenue, and can be used to interpret many facets of neuronal new developments have led to a more in-depth Newark, New Jersey 07102, communication and computation (FIG. 1). A major understanding not only of the relationship between USA. advantage of extracellular field recording techniques is network activity and cognitive behaviour5 but also of 2New York University that, in contrast to several other methods used for the the pathomechanisms in brain diseases6. Neuroscience Institute, New York University Langone investigation of network activity, the biophysics related Several excellent but somewhat dated reviews Medical Center, New York, to these measurements are well understood. This has discuss various aspects of extracellular signals in the – New York 10016, USA. enabled the development of reliable and quantitative brain2,7 25. Here we provide an overview of our present 3Center for Neural Science, mathematical models to elucidate how transmembrane understanding of the mechanisms that underlie New York University, New currents give rise to the recorded electric potential. the generation of extracellular currents and fields. York, New York 10003, USA. 4Division of Biology, Historically, Ve has been referred to as the electro- Although all nervous structures generate extracellular California Institute of encephalogram (EEG) when recorded from the scalp, fields, our focus is the mammalian cerebral cortex, Technology, 1200 East as the electrocorticogram (ECoG) when recorded by as most of our quantitative knowledge is the result of California Boulevard, subdural grid electrodes on the cortical surface, and studies in cortex. Pasadena, California 91125, USA. as the local field potential (LFP; also known as micro-, 1 5Allen Institute for Brain depth or intracranial EEG ) when recorded by a small- Contributors to extracellular fields Science, 551 North 34th size electrode in the brain (BOX 1; FIG. 1). The term ‘local Any excitable membrane — whether it is a spine, Street, Seattle, Washington field potential’ (meaning an electric potential (Ve)), is dendrite, soma, axon or axon terminal — and any 98103, USA. a regrettable malapropism, but we continue to use the type of transmembrane current contributes to the Correspondence to G.B. e-mail: gyorgy.buzsaki@ term LFP because it is familiar to most neuroscientists. extracellular field. The field is the superposition of nyumc.org The magnetic field induced by the same activity is all ionic processes, from fast action potentials to the doi:10.1038/nrn3241 referred to as the magnetoencephalogram (MEG)2. slowest fluctuations in glia. All currents in the brain NATURE REVIEWS | NEUROSCIENCE VOLUME 13 | JUNE 2012 | 407 © 2012 Macmillan Publishers Limited. All rights reserved REVIEWS a b superimpose at any given point in space to yield Ve V at that location. Thus, any transmembrane current, Cz µ Depth irrespective of its origin, leads to an intracellular as 150 (LFP) SM well as an extracellular (that is, LFP) voltage deflection. V µ The characteristics of the LFP waveform, such as the 800 amplitude and frequency, depend on the proportional Grid EC contribution of the multiple sources and various (ECoG) properties of the brain tissue. The larger the distance Strip of the recording electrode from the current source, the (ECoG) HC less informative the measured LFP becomes about the events occurring at the location(s) of the source(s). This Strip is mainly owing to the fact that the V amplitude scales (ECoG) Am e with the inverse of the distance r between the source Fz Scalp and the recording site, and to the inclusion of other EEG O2 (interfering) signals (leading to ‘spatial averaging’). In 1 s 1 s addition to the magnitude and sign of the individual c current sources, and their spatial density, the temporal 1000 100 coordination of the respective current sources (that 500 V) is, their synchrony) shapes the extracellular field. µ Thus, extracellular currents can emerge from multiple 0 0 sources, and these are described below. iEEG ( MEG (fT) –500 –100 –1000 1 s Synaptic activity. In physiological situations, synaptic activity is often the most important source of extracellular current flow. The idea that synaptic d I LFP surface currents contribute to the LFP stems from the II recognition that extracellular currents from many individual compartments must overlap in time to induce III a measurable signal, and such overlap is most easily LFP depth achieved for relatively slow events, such as synaptic 7,10,23 IV Intracellular currents . The dendrites and soma of a neuron form a tree-like structure with an electrically conducting V interior that is surrounded by a relatively insulating 20 mV membrane, with hundreds to tens of thousands of VI synapses located along it. Neurotransmitters acting on Figure 1 | Extracellular traces using different recording methods are synaptic AMPA and NMDA receptors mediate excitatory + 2+ fundamentally similar. a | Simultaneous recordings fromNature three Reviewsdepth electrodes | Neuroscience (two currents, involving Na or Ca ions, respectively, selected sites each) in the left amygdala and hippocampus (measuring the local field which flow inwardly at the synapse. This influx of cations from the extracellular into the intracellular cortex (measuring the electrocorticogram (ECoG); two four-contact strips placed under space gives rise to a local extracellular sink. To achieve the inferior temporal surface (measuring the ECoG); an eight-contact strip placed effective electroneutrality within the time constants of over the left orbitofrontal surface (measuring the ECoG); and scalp electroencephalo- relevance for systems neuroscience, the extracellular graphy (EEG) over both hemispheres (selected sites are the Fz and O2) in a patient with sink needs to be ‘balanced’ by an extracellular source, drug-resistant epilepsy. The amplitude signals are larger and the higher-frequency that is, an opposing ionic flux from the intracellular to patterns have greater resolution at the intracerebral (LFP) and ECoG sites compared to scalp EEG. b | A 6 s epoch of slow waves recorded by scalp EEG (Cz, red), and LFP (blue) the extracellular space, along the neuron; this flux is recorded by depth electrodes placed in the deep layers of the supplementary motor area termed passive current or return current. Depending on (SM) and entorhinal cortex (EC), hippocampus (HC) and amygdala (Am). Also shown are the location of the sink current(s) and its distance from multiple-unit activity (green) and spikes of isolated neurons (black ticks). c | Simultaneously the source current(s), a dipole or a higher-order n-pole recorded magnetoencephalogram (MEG; black) and anterior hippocampus depth EEG is formed (FIG. 2a). The contribution of a monopole to (red) from a patient with drug-resistant epilepsy. Note the similar theta oscillations Ve scales as 1/r, whereas the contribution of a dipole recorded by the depth electrode and the trace calculated by the MEG, without any phase decays faster, as 1/r2; this steeper decay is due to the two delay. d | Simultaneously recorded LFP traces from the superficial (‘surface’) and deep opposing charges that comprise the dipole cancelling (‘depth’) layers of the motor cortex in an anaesthetized cat and an intracellular trace each other out to first order. from a layer 5 pyramidal neuron. Note the alternation of hyperpolarization and Notably, GABA
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