An EEG recording at Dalhousie University
Electroencephalography (EEG) is the recording of electrical activity along the scalp. EEG measures voltage fluctuations resulting from ionic current flows within the neurons of the brain. In clinical contexts, EEG refers to the recording of the brain's spontaneous electrical activity over a short period of time, usually 20–40 minutes, as recorded from multiple electrodes placed on the scalp. Diagnostic applications generally focus on the spectral content of EEG, that is, the type of neural oscillations that can be observed in EEG signals. In neurology, the main diagnostic application of EEG is in the case of epilepsy, as epileptic activity can create clear abnormalities on a standard EEG study. A secondary clinical use of EEG is in the diagnosis of coma, encephalopathies, and brain death. A third clinical use of EEG is for studies of sleep and sleep disorders where recordings are typically done for one full night, sometimes more. EEG used to be a first-line method for the diagnosis of tumors, stroke and other focal brain disorders, but this use has decreased with the advent of anatomical imaging techniques with high (<1 mm) spatial resolution such as MRI and CT. Despite limited spatial resolution, EEG continues to be a valuable tool for research and diagnosis, especially when millisecond-range temporal resolution (not possible with CT or MRI) is required.
Derivatives of the EEG technique include evoked potentials (EP), which involves averaging the EEG activity time-locked to the presentation of a stimulus of some sort (visual, somatosensory, or auditory). Event-related potentials (ERPs) refer to averaged EEG responses that are time-locked to more complex processing of stimuli; this technique is used in cognitive science, cognitive psychology, and psychophysiological research.
A timeline of the history of EEG is given by Swartz. Richard Caton (1842–1926), a physician practicing in Liverpool, presented his findings about electrical phenomena of the exposed cerebral hemispheres of rabbits and monkeys in the British Medical Journal in 1875. In 1890, Polish physiologist Adolf Beck published an investigation of spontaneous electrical activity of the brain of rabbits and dogs that included rhythmic oscillations altered by light.
In 1912, Russian physiologist, Vladimir Vladimirovich Pravdich-Neminsky published the first animal EEG and the evoked potential of the mammalian (dog). In 1914, Napoleon Cybulski and Jelenska-Macieszyna photographed EEG-recordings of experimentally induced seizures.
German physiologist and psychiatrist Hans Berger (1873–1941) recorded the first human EEG in 1924. Expanding on work previously conducted on animals by Richard Caton and others, Berger also invented the electroencephalogram (giving the device its name), an invention described "as one of the most surprising, remarkable, and momentous developments in the history of clinical neurology". His discoveries were first confirmed by British scientists Edgar Douglas Adrian and B. H. C. Matthews in 1934 and developed by them.
In 1934, Fisher and Lowenback first demonstrated epileptiform spikes. In 1935 Gibbs, Davis and Lennox described interictal spike waves and the 3 cycles/s pattern of clinical absence seizures, which began the field of clinical electroencephalography. Subsequently, in 1936 Gibbs and Jasper reported the interictal spike as the focal signature of epilepsy. The same year, the first EEG laboratory opened at Massachusetts General Hospital.
Franklin Offner (1911–1999), professor of biophysics at Northwestern University developed a prototype of the EEG that incorporated a piezoelectric inkwriter called a Crystograph (the whole device was typically known as the Offner Dynograph).
In 1947, The American EEG Society was founded and the first International EEG congress was held. In 1953 Aserinsky and Kleitman describe REM sleep.
In the 1950s, William Grey Walter developed an adjunct to EEG called EEG topography, which allowed for the mapping of electrical activity across the surface of the brain. This enjoyed a brief period of popularity in the 1980s and seemed especially promising for psychiatry. It was never accepted by neurologists and remains primarily a research tool.
The brain's electrical charge is maintained by billions of neurons. Neurons are electrically charged (or "polarized") by membrane transport proteins that pump ions across their membranes. Neurons are constantly exchanging ions with the extracellular milieu, for example to maintain resting potential and to propagate action potentials. Ions of similar charge repel each other, and when many ions are pushed out of many neurons at the same time, they can push their neighbours, who push their neighbours, and so on, in a wave. This process is known as volume conduction. When the wave of ions reaches the electrodes on the scalp, they can push or pull electrons on the metal on the electrodes. Since metal conducts the push and pull of electrons easily, the difference in push or pull voltages between any two electrodes can be measured by a voltmeter. Recording these voltages over time gives us the EEG.
The electric potential generated by single neuron is far too small to be picked up by EEG or MEG. EEG activity therefore always reflects the summation of the synchronous activity of thousands or millions of neurons that have similar spatial orientation. If the cells do not have similar spatial orientation, their ions do not line up and create waves to be detected. Pyramidal neurons of the cortex are thought to produce the most EEG signal because they are well-aligned and fire together. Because voltage fields fall off with the square of distance, activity from deep sources is more difficult to detect than currents near the skull.
Scalp EEG activity shows oscillations at a variety of frequencies. Several of these oscillations have characteristic frequency ranges, spatial distributions and are associated with different states of brain functioning (e.g., waking and the various sleep stages). These oscillations represent synchronized activity over a network of neurons. The neuronal networks underlying some of these oscillations are understood (e.g., the thalamocortical resonance underlying sleep spindles), while many others are not (e.g., the system that generates the posterior basic rhythm). Research that measures both EEG and neuron spiking finds the relationship between the two is complex with the power of surface EEG in only two bands (gamma and delta) relating to neuron spike activity.
A routine clinical EEG recording typically lasts 20–30 minutes (plus preparation time) and usually involves recording from scalp electrodes. Routine EEG is typically used in the following clinical circumstances:
At times, a routine EEG is not sufficient, particularly when it is necessary to record a patient while he/she is having a seizure. In this case, the patient may be admitted to the hospital for days or even weeks, while EEG is constantly being recorded (along with time-synchronized video and audio recording). A recording of an actual seizure (i.e., an ictal recording, rather than an inter-ictal recording of a possibly epileptic patient at some period between seizures) can give significantly better information about whether or not a spell is an epileptic seizure and the focus in the brain from which the seizure activity emanates.
Epilepsy monitoring is typically done:
Additionally, EEG may be used to monitor certain procedures:
EEG can also be used in intensive care units for brain function monitoring:
If a patient with epilepsy is being considered for resective surgery, it is often necessary to localize the focus (source) of the epileptic brain activity with a resolution greater than what is provided by scalp EEG. This is because the cerebrospinal fluid, skull and scalp smear the electrical potentials recorded by scalp EEG. In these cases, neurosurgeons typically implant strips and grids of electrodes (or penetrating depth electrodes) under the dura mater, through either a craniotomy or a burr hole. The recording of these signals is referred to as electrocorticography (ECoG), subdural EEG (sdEEG) or intracranial EEG (icEEG)--all terms for the same thing. The signal recorded from ECoG is on a different scale of activity than the brain activity recorded from scalp EEG. Low voltage, high frequency components that cannot be seen easily (or at all) in scalp EEG can be seen clearly in ECoG. Further, smaller electrodes (which cover a smaller parcel of brain surface) allow even lower voltage, faster components of brain activity to be seen. Some clinical sites record from penetrating microelectrodes.
EEG, and the related study of ERPs are used extensively in neuroscience, cognitive science, cognitive psychology, neurolinguistics and psychophysiological research. Many EEG techniques used in research are not standardized sufficiently for clinical use.
Several other methods to study brain function exist, including functional magnetic resonance imaging (fMRI), positron emission tomography, magnetoencephalography, Nuclear magnetic resonance spectroscopy, Electrocorticography, Single-photon emission computed tomography, Near-infrared spectroscopy (NIRS), and Event-related optical signal (EROS). Despite the relatively poor spatial sensitivity of EEG, it possesses multiple advantages over some of these techniques:
EEG also has some characteristics that compare favorably with behavioral testing:
Simultaneous EEG recordings and fMRI scans have been obtained successfully, though successful simultaneous recording requires that several technical difficulties be overcome, such as the presence of ballistocardiographic artifact, MRI pulse artifact and the induction of electrical currents in EEG wires that move within the strong magnetic fields of the MRI. While challenging, these have been successfully overcome in a number of studies.
Similarly, simultaneous recordings with MEG and EEG have also been conducted, which has several advantages over using either technique alone:
EEG has also been combined with positron emission tomography. This provides the advantage of allowing researchers to see what EEG signals are associated with different drug actions in the brain.
In conventional scalp EEG, the recording is obtained by placing electrodes on the scalp with a conductive gel or paste, usually after preparing the scalp area by light abrasion to reduce impedance due to dead skin cells. Many systems typically use electrodes, each of which is attached to an individual wire. Some systems use caps or nets into which electrodes are embedded; this is particularly common when high-density arrays of electrodes are needed.
Electrode locations and names are specified by the International 10–20 system for most clinical and research applications (except when high-density arrays are used). This system ensures that the naming of electrodes is consistent across laboratories. In most clinical applications, 19 recording electrodes (plus ground and system reference) are used. A smaller number of electrodes are typically used when recording EEG from neonates. Additional electrodes can be added to the standard set-up when a clinical or research application demands increased spatial resolution for a particular area of the brain. High-density arrays (typically via cap or net) can contain up to 256 electrodes more-or-less evenly spaced around the scalp.
Each electrode is connected to one input of a differential amplifier (one amplifier per pair of electrodes); a common system reference electrode is connected to the other input of each differential amplifier. These amplifiers amplify the voltage between the active electrode and the reference (typically 1,000–100,000 times, or 60–100 dB of voltage gain). In analog EEG, the signal is then filtered (next paragraph), and the EEG signal is output as the deflection of pens as paper passes underneath. Most EEG systems these days, however, are digital, and the amplified signal is digitized via an analog-to-digital converter, after being passed through an anti-aliasing filter. Analog-to-digital sampling typically occurs at 256–512 Hz in clinical scalp EEG; sampling rates of up to 20 kHz are used in some research applications.
During the recording, a series of activation procedures may be used. These procedures may induce normal or abnormal EEG activity that might not otherwise be seen. These procedures include hyperventilation, photic stimulation (with a strobe light), eye closure, mental activity, sleep and sleep deprivation. During (inpatient) epilepsy monitoring, a patient's typical seizure medications may be withdrawn.
The digital EEG signal is stored electronically and can be filtered for display. Typical settings for the high-pass filter and a low-pass filter are 0.5-1 Hz and 35–70 Hz, respectively. The high-pass filter typically filters out slow artifact, such as electrogalvanic signals and movement artifact, whereas the low-pass filter filters out high-frequency artifacts, such as electromyographic signals. An additional notch filter is typically used to remove artifact caused by electrical power lines (60 Hz in the United States and 50 Hz in many other countries). As part of an evaluation for epilepsy surgery, it may be necessary to insert electrodes near the surface of the brain, under the surface of the dura mater. This is accomplished via burr hole or craniotomy. This is referred to variously as "electrocorticography (ECoG)", "intracranial EEG (I-EEG)" or "subdural EEG (SD-EEG)". Depth electrodes may also be placed into brain structures, such as the amygdala or hippocampus, structures, which are common epileptic foci and may not be "seen" clearly by scalp EEG. The electrocorticographic signal is processed in the same manner as digital scalp EEG (above), with a couple of caveats. ECoG is typically recorded at higher sampling rates than scalp EEG because of the requirements of Nyquist theorem-the subdural signal is composed of a higher predominance of higher frequency components. Also, many of the artifacts that affect scalp EEG do not impact ECoG, and therefore display filtering is often not needed.
A typical adult human EEG signal is about 10 µV to 100 µV in amplitude when measured from the scalp and is about 10–20 mV when measured from subdural electrodes.
The EEG recording can be analysed using various programs; e.g., using free open-source toolboxes for Matlab, such as, EEGLAB, Fieldtrip, NBT, SPM, or commercial software packages such as Brainvision Analyzer.
Since an EEG voltage signal represents a difference between the voltages at two electrodes, the display of the EEG for the reading encephalographer may be set up in one of several ways. The representation of the EEG channels is referred to as a montage.
When analog (paper) EEGs are used, the technologist switches between montages during the recording in order to highlight or better characterize certain features of the EEG. With digital EEG, all signals are typically digitized and stored in a particular (usually referential) montage; since any montage can be constructed mathematically from any other, the EEG can be viewed by the electroencephalographer in any display montage that is desired.
The EEG is read by a clinical neurophysiologist or neurologist (depending on local custom and law regarding medical specialities), optimally one who has specific training in the interpretation of EEGs for clinical purposes. This is done by visual inspection of the waveforms, called graphoelements. The use of computer signal processing of the EEG-so-called quantitative EEG-is somewhat controversial when used for clinical purposes (although there are many research uses).
EEG has several limitations. Most important is its poor spatial resolution. EEG is most sensitive to a particular set of post-synaptic potentials: those generated in superficial layers of the cortex, on the crests of gyri directly abutting the skull and radial to the skull. Dendrites, which are deeper in the cortex, inside sulci, in midline or deep structures (such as the cingulate gyrus or hippocampus), or producing currents that are tangential to the skull, have far less contribution to the EEG signal.
It is mathematically impossible to reconstruct a unique intracranial current source for a given EEG signal, as some currents produce potentials that cancel each other out. This is referred to as the inverse problem. However, much work has been done to produce remarkably good estimates of, at least, a localized electric dipole that represents the recorded currents.
EEG has several strong points as a tool for exploring brain activity. EEG's can detect changes over milliseconds, which is excellent considering an action potential takes approximately 0.5-130 milliseconds to propagate across a single neuron, depending on the type of neuron. Other methods of looking at brain activity, such as PET and fMRI have time resolution between seconds and minutes. EEG measures the brain's electrical activity directly, while other methods record changes in blood flow (e.g., SPECT, fMRI) or metabolic activity (e.g., PET, NIRS), which are indirect markers of brain electrical activity. EEG can be used simultaneously with fMRI so that high-temporal-resolution data can be recorded at the same time as high-spatial-resolution data, however, since the data derived from each occurs over a different time course, the data sets do not necessarily represent exactly the same brain activity. There are technical difficulties associated with combining these two modalities, including the need to remove the MRI gradient artifact present during MRI acquisition and the ballistocardiographic artifact (resulting from the pulsatile motion of blood and tissue) from the EEG. Furthermore, currents can be induced in moving EEG electrode wires due to the magnetic field of the MRI. EEG can be used simultaneously with NIRS without major technical difficulties. There is no influence of these modalities on each other and a combined measurement can give useful information about electrical activity as well as local hemodynamics.
EEG reflects correlated synaptic activity caused by post-synaptic potentials of cortical neurons. The ionic currents involved in the generation of fast action potentials may not contribute greatly to the averaged field potentials representing the EEG . More specifically, the scalp electrical potentials that produce EEG are generally thought to be caused by the extracellular ionic currents caused by dendritic electrical activity, whereas the fields producing magnetoencephalographic signals are associated with intracellular ionic currents .
EEG can be recorded at the same time as MEG so that data from these complementary high-time-resolution techniques can be combined.
The EEG is typically described in terms of (1) rhythmic activity and (2) transients. The rhythmic activity is divided into bands by frequency. To some degree, these frequency bands are a matter of nomenclature (i.e., any rhythmic activity between 6–12 Hz can be described as "alpha"), but these designations arose because rhythmic activity within a certain frequency range was noted to have a certain distribution over the scalp or a certain biological significance. Frequency bands are usually extracted using spectral methods (for instance Welch) as implemented for instance in freely available EEG software such as EEGLAB or the the neurophysiological biomarker toolbox.
Most of the cerebral signal observed in the scalp EEG falls in the range of 1–20 Hz (activity below or above this range is likely to be artifactual, under standard clinical recording techniques).
|Delta||up to 4||frontally in adults, posteriorly in children; high-amplitude waves||
|Theta||4 – 8||Found in locations not related to task at hand||
|Alpha||8 – 13||posterior regions of head, both sides, higher in amplitude on non-dominant side. Central sites (c3-c4) at rest||
|Beta||>13 – 30||both sides, symmetrical distribution, most evident frontally; low-amplitude waves||
|Gamma||30 – 100+||Somatosensory cortex||
|Mu||8 – 13||Sensorimotor cortex||
While these are the universally recognized frequency ranges that researchers tend to follow, many scholars use their own specific range boundaries depending on the frequencies they choose to focus on. Additionally, some researchers define the bands using decimal values rather than rounding to whole numbers (for example, one researcher may define the lower Beta band cut-off as 12.1, while another may use the value 13), while still others sometimes divide the bands into subbands for the purposes of data analysis.
"Ultra-slow" or "near-DC" (Direct current) activity is recorded using DC amplifiers in some research contexts. It is not typically recorded in a clinical context because the signal at these frequencies is susceptible to a number of artifacts.
Some features of the EEG are transient rather than rhythmic. Spikes and sharp waves may represent seizure activity or interictal activity in individuals with epilepsy or a predisposition toward epilepsy. Other transient features are normal: vertex waves and sleep spindles are seen in normal sleep.
Note that there are types of activity that are statistically uncommon, but not associated with dysfunction or disease. These are often referred to as "normal variants." The mu rhythm is an example of a normal variant.
The normal Electroencephalography (EEG) varies by age. The neonatal EEG is quite different from the adult EEG. The EEG in childhood generally has slower frequency oscillations than the adult EEG.
The normal EEG also varies depending on state. The EEG is used along with other measurements (EOG, EMG) to define sleep stages in polysomnography. Stage I sleep (equivalent to drowsiness in some systems) appears on the EEG as drop-out of the posterior basic rhythm. There can be an increase in theta frequencies. Santamaria and Chiappa cataloged a number of the variety of patterns associated with drowsiness. Stage II sleep is characterized by sleep spindles-transient runs of rhythmic activity in the 12–14 Hz range (sometimes referred to as the "sigma" band) that have a frontal-central maximum. Most of the activity in Stage II is in the 3–6 Hz range. Stage III and IV sleep are defined by the presence of delta frequencies and are often referred to collectively as "slow-wave sleep." Stages I-IV comprise non-REM (or "NREM") sleep. The EEG in REM (rapid eye movement) sleep appears somewhat similar to the awake EEG.
EEG under general anesthesia depends on the type of anesthetic employed. With halogenated anesthetics, such as halothane or intravenous agents, such as propofol, a rapid (alpha or low beta), nonreactive EEG pattern is seen over most of the scalp, especially anteriorly; in some older terminology this was known as a WAR (widespread anterior rapid) pattern, contrasted with a WAIS (widespread slow) pattern associated with high doses of opiates. Anesthetic effects on EEG signals are beginning to be understood at the level of drug actions on different kinds of synapses and the circuits that allow synchronized neuronal activity (see: http://www.stanford.edu/group/maciverlab/).
Electrical signals detected along the scalp by an EEG, but that originate from non-cerebral origin are called artifacts. EEG data is almost always contaminated by such artifacts. The amplitude of artifacts can be quite large relative to the size of amplitude of the cortical signals of interest. This is one of the reasons why it takes considerable experience to correctly interpret EEGs clinically. Some of the most common types of biological artifacts include:
The most prominent eye-induced artifacts are caused by the potential difference between the cornea and retina, which is quite large compared to cerebral potentials. When the eyes and eyelids are completely still, this corneo-retinal dipole does not affect EEG. However, blinks occur several times per minute, the eyes movements occur several times per second. Eyelid movements, occurring mostly during blinking or vertical eye movements, elicit a large potential seen mostly in the difference between the Electrooculography (EOG) channels above and below the eyes. An established explanation of this potential regards the eyelids as sliding electrodes that short-circuit the positively charged cornea to the extra-ocular skin. Rotation of the eyeballs, and consequently of the corneo-retinal dipole, increases the potential in electrodes towards which the eyes are rotated, and decrease the potentials in the opposing electrodes. Eye movements called saccades also generate transient electromyographic potentials, known as saccadic spike potentials (SPs). The spectrum of these SPs overlaps the gamma-band (see Gamma wave), and seriously confounds analysis of induced gamma-band responses, requiring tailored artifact correction approaches. Purposeful or reflexive eye blinking also generates electromyographic potentials, but more importantly there is reflexive movement of the eyeball during blinking that gives a characteristic artifactual appearance of the EEG (see Bell's phenomenon).
Eyelid fluttering artifacts of a characteristic type were previously called Kappa rhythm (or Kappa waves). It is usually seen in the prefrontal leads, that is, just over the eyes. Sometimes they are seen with mental activity. They are usually in the Theta (4–7 Hz) or Alpha (8–13 Hz) range. They were named because they were believed to originate from the brain. Later study revealed they were generated by rapid fluttering of the eyelids, sometimes so minute that it was difficult to see. They are in fact noise in the EEG reading, and should not technically be called a rhythm or wave. Therefore, current usage in electroencephalography refers to the phenomenon as an eyelid fluttering artifact, rather than a Kappa rhythm (or wave).
Some of these artifacts can be useful in various applications. The EOG signals, for instance, can be used to detect and track eye-movements, which are very important in polysomnography, and is also in conventional EEG for assessing possible changes in alertness, drowsiness or sleep.
EKG artifacts are quite common and can be mistaken for spike activity. Because of this, modern EEG acquisition commonly includes a one-channel EKG from the extremities. This also allows the EEG to identify cardiac arrhythmias that are an important differential diagnosis to syncope or other episodic/attack disorders.
Glossokinetic artifacts are caused by the potential difference between the base and the tip of the tongue. Minor tongue movements can contaminate the EEG, especially in parkinsonian and tremor disorders.
In addition to artifacts generated by the body, many artifacts originate from outside the body. Movement by the patient, or even just settling of the electrodes, may cause electrode pops, spikes originating from a momentary change in the impedance of a given electrode. Poor grounding of the EEG electrodes can cause significant 50 or 60 Hz artifact, depending on the local power system's frequency. A third source of possible interference can be the presence of an IV drip; such devices can cause rhythmic, fast, low-voltage bursts, which may be confused for spikes.
Recently, independent component analysis techniques have been used to correct or remove EEG contaminates. These techniques attempt to "unmix" the EEG signals into some number of underlying components. There are many source separation algorithms, often assuming various behaviors or natures of EEG. Regardless, the principle behind any particular method usually allow "remixing" only those components that would result in "clean" EEG by nullifying (zeroing) the weight of unwanted components. Fully automated artifact rejection methods, which use ICA, have also been developed.
Abnormal activity can broadly be separated into epileptiform and non-epileptiform activity. It can also be separated into focal or diffuse.
Focal epileptiform discharges represent fast, synchronous potentials in a large number of neurons in a somewhat discrete area of the brain. These can occur as interictal activity, between seizures, and represent an area of cortical irritability that may be predisposed to producing epileptic seizures. Interictal discharges are not wholly reliable for determining whether a patient has epilepsy nor where his/her seizure might originate. (See focal epilepsy.)
Generalized epileptiform discharges often have an anterior maximum, but these are seen synchronously throughout the entire brain. They are strongly suggestive of a generalized epilepsy.
Focal non-epileptiform abnormal activity may occur over areas of the brain where there is focal damage of the cortex or white matter. It often consists of an increase in slow frequency rhythms and/or a loss of normal higher frequency rhythms. It may also appear as focal or unilateral decrease in amplitude of the EEG signal.
Diffuse non-epileptiform abnormal activity may manifest as diffuse abnormally slow rhythms or bilateral slowing of normal rhythms, such as the PBR.
Intracortical Encephalogram electrodes and sub-dural electrodes can be used in tandem to discriminate and discretize artifact from epileptiform and other severe neurological events.
More advanced measures of abnormal EEG signals have also recently received attention as possible biomarkers for different disorders such as Alzheimer's disease.
The EEG has been used for many purposes besides the conventional uses of clinical diagnosis and conventional cognitive neuroscience. An early use was during World War II by the U.S. Army Air Corps to screen out pilots in danger of having seizures; long-term EEG recordings in epilepsy patients are still used today for seizure prediction. Neurofeedback remains an important extension, and in its most advanced form is also attempted as the basis of brain computer interfaces. The EEG is also used quite extensively in the field of neuromarketing.
Honda is attempting to develop a system to enable an operator to control its Asimo robot using EEG, a technology it eventually hopes to incorporate into its automobiles.
The United States Army Research Office budgeted $4 million in 2009 to researchers at the University of California, Irvine to develop EEG processing techniques to identify correlates of imagined speech and intended direction to enable soldiers on the battlefield to communicate via computer-mediated reconstruction of team members' EEG signals, in the form of understandable signals such as words.
Inexpensive EEG devices exist for the low-cost research and consumer markets. Recently, a few companies have miniaturized medical grade EEG technology to create versions accessible to the wider public. Some of these companies have even built commercial EEG devices retailing for less than $100 USD.
EEG electroencephalophone used during a music performance in which bathers from around the world were networked together as part of a collective musical performance, using their brainwaves to control sound, lighting, and the bath environment
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