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  • Review Article
  • Published:

The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes

Nature Reviews Neuroscience volume 13, pages 407–420 (2012)Cite this article

Subjects

Key Points

  • All currents in the brain superimpose to yield an 'electric field' at any given point in space. The current sources and sinks form dipoles or higher-order n-poles.

  • Extracellular currents arise from many sources, including synaptic currents, fast action potentials and their afterpotentials, calcium spikes and voltage-dependent intrinsic currents.

  • The magnitude of extracellular currents depends critically on two factors: the cytoarchitectural organization of a network and the temporal synchrony of the various current sinks and sources.

  • Depending on the recording method, neuroscientists distinguish between electroencephalogram (EEG), electrocorticogram (ECoG) and local field potential (LFP; also known as micro-, depth or intracranial EEG), although all of these measures refer to the same biophysical process.

  • The electric field is the force 'felt' by an electric charge, and can be transmitted through brain volume. The extent of volume conduction depends on the relationships between the current dipole and the features of the conductive medium.

  • High-density sampling of the extracellular field with contemporary methods enables the calculation of current source density, and therefore the localization of current sinks and sources.

  • The voltage gradients generated by highly synchronous activity of neuronal groups can affect the transmembrane potential of the member neurons and alter their excitability through ephaptic coupling.

  • Synchronous spiking of nearby neurons is the main source of the high-frequency components of the local field.

  • There is a discernable relationship between the temporal evolution of cell assemblies and the time-dependent changes of the spatially distributed currents. High-density, wide-band recordings of the local field can therefore provide access to both afferent inputs and the spiking output of neurons.

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.

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Figure 1: Extracellular traces using different recording methods are fundamentally similar.
Figure 2: Excitatory and inhibitory postsynaptic currents are the most ubiquitous contributors to Ve.
Figure 3: Non-synaptic contributions to the LFP.
Figure 4: Identifying current sources.
Figure 5: Spike contribution to the LFP.
Figure 6: Spikes are embedded in unique synapsembles and spatially distributed LFP.

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Acknowledgements

The authors are supported by the National Institutes of Health (grants NS34994, MH54671 and NS074015), the Swiss National Science Foundation (grant PA00P3_131470), the G. Harold and Leila Y. Mathers Charitable Foundation, the US–Israel Binational Foundation, the Global Institute for Scientific Thinking and the Human Frontiers Science Program (grant RGP0032/2011). Parts of this Review were written while G.B. was a visiting scholar at the Interdisciplinary Center for Neural Computation, Hebrew University, Jerusalem (2007) and at the Zukunftskolleg Program, University of Konstanz, Germany (2011). We thank G. Einevoll, E. Schomburg and J. Taxidis for their comments on the manuscript.

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Authors and Affiliations

  1. Center for Molecular and Behavioural Neuroscience, Rutgers, The State University of New Jersey, 197 University Avenue, Newark, 07102, New Jersey, USA

    György Buzsáki

  2. New York University Neuroscience Institute, New York University Langone Medical Center, New York, 10016, New York, USA

    György Buzsáki

  3. Center for Neural Science, New York University, New York, 10003, New York, USA

    György Buzsáki

  4. Division of Biology, California Institute of Technology, 1200 East California Boulevard, Pasadena, 91125, California, USA

    Costas A. Anastassiou & Christof Koch

  5. Allen Institute for Brain Science, 551 North 34th Street, Seattle, 98103, Washington, USA

    Christof Koch

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Correspondence to György Buzsáki.

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Supplementary information

Supplementary Information S1 (movie)

Spike-triggered average of the LFP in the hippocampus during exploration. (AVI 3003 kb)

Supplementary Information S2 (movie)

Spike triggered average of the LFP in the hippocampus during non-REM sleep. (AVI 3033 kb)

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Glossary

Sink

By convention, a site on the neuronal membrane where positive charges enter the neuron.

Electroneutrality

The phenomenon that, owing to charge conservation, at any given point in time the total charge entering and leaving the cell across all of its membrane equals zero.

Sources

Locations along the neuronal membrane where positive charge flows out of the neuron. For negative charge, the location of sinks and sources is inverted.

Return current

A loop current that flows in the opposite direction to an active sink or source.

Dipole

An ideal electric dipole is defined by two charges of opposite polarity with infinitely small separation, such that the product of the charge times the distance r separating them remains finite. The electric potential of a dipole falls off as 1/r2.

Equilibrium potential

The voltage difference between intracellular and extracellular space of a neuron when the net ionic flux across the membrane equals zero.

Ih currents

Currents flowing through hyperpolarization deinactivated cyclic nucleotide-gated channels.

IT currents

Low-threshold (hyperpolarization-induced) transient Ca2+ currents, which often lead to burst firing.

Resonance

A property of the neuronal membrane to respond to some input frequencies more strongly than others. At the resonant frequency, even weak periodic driving can produce large-amplitude oscillations.

Silicon probes

Multiple-site recording electrodes for high spatial density monitoring of the extracellular field. The recordings sites can record Ve along one, two or even three orthogonal axes.

Ephaptic coupling

The effect of the extracellular field on the transmembrane potential of a neuron.

Open field

When the sink (or the source) is substantially spatially separated from the return currents of the dipole.

Closed field

When the sink (or the source) is minimally spatially separated from the return currents of the dipole.

Power law (of LFP)

The power law of LFP describes a relationship between the amplitude of the extracellular signal and its temporal frequency. A descending straight line on the log–log plot (power versus frequency) would be an indication of a power law that scales as 1/fn.

Low-pass frequency filtering

A process by which the frequency components of a signal beyond a cutoff frequency are increasingly attenuated, typically owing to a serial capacitance (for example, the bi-lipid membrane).

Phase–amplitude coupling

The power of a faster oscillation is phase-modulated by a slower oscillation.

Ohmic

Electrical current flow through a purely resistive milieu. The extracellular cytoplasm is primarily ohmic in the 1–10,000 kHz frequency range.

Current source density

(CSD). The current source density reflects the rate of current flow in a given direction through the unit surface (unit, A m−2) or volume (unit, A m−3).

Anisotropic

Ansiotropic tissue can conduct electricity in a direction-dependent manner.

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Buzsáki, G., Anastassiou, C. & Koch, C. The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes. Nat Rev Neurosci 13, 407–420 (2012). https://doi.org/10.1038/nrn3241

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