Electrical activity in the brain, which is what an EEG records, was first measured in 1875 by Richard Caton, who noted the electrical oscillations on the exposed cortical surface of animals. The physiologic mechanisms and cortical morphology responsible for generating the EEG are presented by Martin,1 and some essential features are summarized here.
Neural Basis of Electroencephalography
The EEG is derived from postsynaptic potentials on pyramidal cells. There are 2 major classes of cortical neurons, pyramidal and nonpyramidal. Pyramidal cells derive their name from their distinctive shape and are notable as the only neuron that projects axons out of the cerebral cortex and locally as well. Their apical dendritic spines are oriented perpendicularly to the cortical surface and extend through the lamina of the cortex, enabling connection with all of the nonpyramidal cortical cells. These nonpyramidal cells serve to modulate pyramidal cell output through stimulation (glutamate alteration of postsynaptic potential) or inhibition (GABA [γ-aminobutyric acid] alteration of postsynaptic potentials) (Fig. 33-1 and Table 33-1).
Schematic of cortical pyramidal, basket, and inter neurons. [From Martin JH. The collective electrical behavior of cortical neurons: The electroencephalogram and the mechanisms of epilepsy. In: Kandel ER, Schwartz JH, Jessel TM, eds. Principles of Neural Science. 3rd ed. New York, Amsterdam, London, Tokyo: Elsevier; 1991:777-791.]
Table 33-1 Cortical Neurons Contributing to Generation of the Electroencephalogram ||Download (.pdf)
Table 33-1 Cortical Neurons Contributing to Generation of the Electroencephalogram
|Neuron||Cytologic Features||Synapses With||Neurotransmitter||Stimulates or Inhibits Target Neuron|
Only output neurons of the cortex
No dendritic spines
Pyramidal cell dendrites
Envelops the soma of postsynaptic cell bodies, hence the name basket
Pyramidal cell bodies, hence the name basket
Pericolumnar inhibition enabling neurons in a given cortical column to function in relative isolation from neighboring columns
Collective voltage of cortical neuron ensembles is measurable at the scalp. The parallel orientation of the pyramidal cells enables the constructive addition of polarity from each cell to be measured at the surface of the cerebral cortex (Fig. 33-2).
Scalp voltage potential depends on perpendicular orientation of pyramidal cells and the polarity of the apical dendrites. [From Martin JH. The collective electrical behavior of cortical neurons: The electroencephalogram and the mechanisms of epilepsy. In: Kandel ER, Schwartz JH, Jessel TM, eds. Principles of Neural Science. 3rd ed. New York, Amsterdam, London, Tokyo: Elsevier; 1991:777-791.]
Because the postsynaptic potentials last for a relatively long period of time and are geometrically aligned, it is possible for the potentials to summate to a sufficiently large magnitude to be measurable by electrodes placed on the scalp. Action potentials, which are of a much larger magnitude than the postsynaptic potential, are too brief to enable summation and therefore do not contribute to the EEG. Similar mechanisms for the generation of the EEG are presented by Rampil,2 Lukatch and Greenwald,3 and McPherson.4 The EEG is an electrical potential versus time measurement that measures cortical voltages at the scalp resulting from the collective postsynaptic potentials of ensembles of cortical pyramidal cells.
Synchronous versus Desynchronous Electroencephalographic Patterns
This cellular mechanism forms the conceptual basis of 2 basic patterns of EEG, synchronous and desynchronous EEG. A synchronous EEG is composed of large-amplitude peaks with slow-frequency oscillations. Referring to the basic mechanism presented previously, a synchronous EEG results when an ensemble of many cortical dendrites are polarized in synchrony. The voltage amplitude is large because the individual depolarizations are additive. The thalamus serves as the orchestrator of pyramidal cell depolarization during EEG synchrony, and the frequency of thalamic stimulation determines the slow rate of cortical polarization or depolarization.5 A desynchronous EEG results when cortical dendrites are polarized by a less circumscribed group of afferent nerves. The consequence of diverse sources of polarizations is a faster frequency of oscillation. The polarizations are not additive and therefore are of lower amplitude. Drawing from this conceptual framework, certain patterns are evident in the normal waking and sleeping EEG (Fig. 33-3). A normal EEG from an awake, alert person is characterized by irregular EEG oscillations with a variable frequency greater than 12 cycles/s and relatively small amplitude. Low-amplitude, high-frequency EEG activity, the hallmark of desynchronous EEG, is the typical EEG pattern of the awake and dreaming brain (the consciously perceiving brain). Departures from normal waking consciousness during sleep are characterized by a slowing of the oscillation frequency and an increase in amplitude of the voltage oscillation. Neuronal discharge is no longer subject to the ambient environmental stimuli–responses characteristics of wakefulness. Orchestration of neuronal discharge is now directed by central pattern generators (presumably located in the thalamus).5 The constructive interference of these waves is evidenced by large-amplitude and slow-frequency EEG traces, the hallmark of the synchronized EEG of the sleeping brain.
Electroencephalographic patterns from wakefulness (desynchrony) to sleep (synchrony) to dreaming (desynchrony). [From PowerPoint presentation: Sleep and Epilepsy in Childhood by Lawrence W. Brown, MD Co-Director, Pediatric Neuropsychiatry Program Co-Director, Pediatric Regional Epilepsy Program, The Children's Hospital of Philadelphia. www.aesnet.org/visitors/ProfessionalDevelopment/Educational/documents/Sleep_Epilepsy.ppt Website for the American Epilepsy Society.]
Desynchronous Electroencephalography: Wakefulness and REM Sleep
One of the early findings in sleep research was that the EEG reverted from a synchronous pattern (low frequency, large amplitude) to a desynchronous pattern when a subject passed from non–rapid eye movement (NREM) sleep to rapid eye movement (REM) sleep. Because subjects were able to report dreams (cognitive activity) at the conclusion of these episodes and because awake patients also demonstrated desynchronous EEGs, the notion that EEG desynchrony was the electrical correlate of a cognitively functioning brain. Conversely, EEG synchrony was the hallmark of the unconscious brain. The transition from desynchronous EEG to synchronous EEG during sleep onset is characterized by the gradual appearance of slow oscillations in the EEG. The tendency for an EEG to develop a synchronous pattern is also known as slowing.
Synchronous Electroencephalography: Natural Sleep, Drug-Induced Sedation, "Light" Anesthesia, and Cerebral Ischemia
All of these states are usually marked by an alteration of consciousness. But all of these states are not equivalent in terms of the degree of altered wakefulness or in terms of the likelihood of return to normal consciousness. However, for all of these states, a return to normal waking consciousness is associated with a return of a desynchronized EEG pattern. In summary, the synchronous EEG does not specifically identify the cause of the EEG synchrony (and its associated alteration of consciousness). Therefore, synchronous EEG will be less than specific in predicting the consequences.6
The following 4 points, although highly simplified, represent key concepts in EEG generation: (1) EEG signals recorded at the skull surface represent the summated postsynaptic potential of hundreds of thousands to millions of pyramidal neurons. (2) Although EEG rhythms recorded at the skull surface are generated by neocortical neurons, these rhythms may originate either in the neocortex itself, or they may be "imposed on" the neocortex by subcortical structures that "pace" the activity of neocortical neurons. (3) Multiple neurotransmitter systems can be involved in generating different types of EEG activity. (4) EEG activity within individual frequency bands (ie, delta, theta, alpha, beta, or gamma) likely represents more than 1 phenomenon."3
Studies Suggesting the Cellular Mechanisms for Electroencephalographic Synchrony: How Sleep, Anesthesia, and Cerebral Lesions Slow the Electroencephalogram
Amzica and Steriade5 have reviewed the evidence for the cellular mechanisms of slow wave generation during natural sleep. Their summary describes 3 different oscillations that "coalesce into the polymorphic wave of slow wave EEG sleep" (Fig. 33-4). Salient points from their review include
Cellular discharge data are obtained from cats anesthetized with ketamine and xylazine. Therefore, there is a leap of faith that the mechanism of slowing from sleep versus anesthesia is the same.
Human data during natural sleep are not obtained from single-cell but from scalp EEG. Therefore, there is an assumption that cellular data from anesthetized cats can be extrapolated to unmeasured cellular phenomena of sleeping humans because of a similarity of the EEGs from both groups.
Deafferented cortex (cortex disconnected from thalamic input by surgical prep or tumor) tends to reveal a slow wave pattern.
Cortical and thalamic depolarization leading to delta slow waves. EEG, electroencephalogram. [From Amzica F, Steriade M. Electrophysiological correlates of sleep delta waves. Electroencephalogr Clin Neurophysiol. 1998;107:69-83.]
The EPITIDE (enhanced phasic inhibition, tonic inhibition, and depressed excitation) theory of anesthetic action on patterned brain activity proposes that anesthetic-induced prolongation of inhibitory currents may slow EEG activity by limiting neuronal discharge frequencies of EEG-generating neurons. Lukatch and Greenwald3 propose that the origin of the EEG rhythms arise in neocortical neurons and may also be "imposed" on neocortical neurons by subcortical structures that "pace" the cortex. Multiple neurotransmitter systems are involved, and EEG activity within individual frequency bands likely represents more than 1 phenomenon. The anesthetic effect on EEG is not a simple transition from the desynchronized EEG to the synchronous but rather involves an initial EEG activation at subanesthetic concentrations (perhaps an EEG correlate of the clinical excitement phase of subanesthetic levels during induction and emergence). At greater anesthetic exposure, the EEG evolves into a synchronous pattern of slowing followed at even greater exposure by isoelectric EEG with bursts of oscillation. It is hypothesized that at the network level, this cellular effect could produce a state in which low-frequency EEG oscillations (eg, delta activity) are supported by the network but higher-frequency oscillations are filtered out (much like the activity of a low-pass filter in an electronics circuit). Lukatch and Greenwald3 state that the theory relies on anesthetic effect on the cortical networks to explain the EEG effect. The theory does not address the role of subcortical networks of cortical slowing proposed for the mechanism of natural sleep-related EEG slowing. Further observations are required for confirmation.
Electroencephalographic changes induced by a variety of insults include EEG slowing, burst suppression, and isoelectric activity. Neuronal electrophysiologic changes responsible for these EEG changes were explored by Rabinovici et al7 This study used an in vitro rat brain slice model that enabled the measurement of single-cell discharge and simultaneous cortical field potential (analogous to EEG) resulting from exposure to the brain slice to hypoxia, ischemia, and hypoglycemia. The findings show that EEG slowing, burst suppression, and isoelectric EEG occur with varying patterns depending on the lesion and that some patterns of damage occur with recovery from the insult. This study did not specifically address the role of subcortical structures (ie, thalamus) in the generation of slowed EEG, suggesting that thalamic mechanisms may not be necessary for the genesis of a slowed EEG in response to cerebral insult.
The work of Amzica and Steriade5, Lukatch and Greenwald,3 and Rabinovici et al7 illustrates that ischemia, hypoxia, hypoglycemia, and anesthesia produce cortical EEG slowing by a variety cellular electrophysiologic mechanisms that may not be distinguishable from the macroscopic EEG.
Intraoperative Electroencephalography Uses
The foregoing discussion indicates that a variety of "natural," pharmacologic, and pathologic causes alter conscious brain function and the associated EEG. This overlap points to the necessity of obtaining confirmatory data to determine the cause and treatment of such EEG changes.
The EEG is not homogeneous throughout the skull (Fig. 33-5). The EEG activity varies considerably depending on the location of the electrode pair being monitored. Therefore, a standardized scheme of electrode application, the 10-20-20 system, has been developed to more reliably position EEG sensing electrodes using surface landmarks of the head for reference points. This reference system enables electrode to be placed at positions that are likely to detect EEG changes because of alteration of local perfusion evoked EEG changes because of stimulation of a particular extremity (Fig. 33-6).
Heterogeneous appearance of electroencephalograms obtained simultaneously from many sites on the scalp. [Modified from Mahla M, Black S, Cucchira R. Neurologic Monitoring Miller's Anesthesia. 6th ed. Philadelphia, PA Churchill Livingstone; 2005:1511-1550.]
10-20-20 system highlighting the position of electrodes to underline cortical anatomy. [From Keifer JC. Somatosensory evoked potentials. In: Russel GB, Rodichok LD, eds. Intraoperative Neurophysiologic Monitoring. Boston, MA: Butterworth-Heineman; 1995:125-333.]
Doubt has been cast8 on the standard 10-20-20 system to have sufficient spatial sensitivity to determine small areas of cerebral ischemia. The EEG, however, is symmetric about the midline with EEG activity on 1 hemisphere generating a "mirror image" of the same area on the other side of the midline. This feature adds a benefit of internal control when assessing changes in an area of EEG activity. If the mirror image area of 1 hemisphere does not mimic the change on the other side, then the change is focal and likely attributable to a change in the activity of the area under monitoring. Symmetric changes in the EEGs of both hemispheres' activity suggest a global source of altered neural activity and therefore more likely attributable to global changes (ie, blood pressure, oxygenation, anesthetic depth). The converse is also true. Focal changes in EEG activity over 1 portion of the brain may not be detected over another portion of the same brain. This fact has consequence when one tries to describe a global change in cerebral activity from 1 focal electrode pair. At least 2 electrode pairs from mirror image sites on either cortex are necessary to conclude that a particular EEG change reflects a "global" change in activity.
The ischemic effect of carotid cross-clamping was reported by Chiappa et al in 19709 (Table 33-2). There was a variety of postclamping patterns. The changes were not global but reflected local changes in activity, underscoring the importance of a symmetric array of electrodes to detect changes over 1 hemisphere versus the other. EEG changes were sometimes observed over the cerebral hemisphere opposite to the clamped side, suggesting an interruption of collateral circulation.
Table 33-2 Summary of Electroencephalographic Changes in 36 of 367 (9.8%) Human Endarterectomy Patients ||Download (.pdf)
Table 33-2 Summary of Electroencephalographic Changes in 36 of 367 (9.8%) Human Endarterectomy Patients
|Group||Decreased Voltage||Decreased Frequency||Ipsilateral||Bilateral||Immediate||Delayed|
A Cochrane meta-analysis10 reviewed 2 prospective randomized studies (composed of 590 patients) that compared routine selective shunting strategy with a no shunt strategy for carotid endarterectomy (CEA). The analysis reviewed a third study that explored the potential benefit of intraoperative EEG monitoring to identify CEA patients who would benefit from shunting. The authors concluded: "There is still insufficient evidence from randomized controlled trials to support or refute the use of routine or selective shunting during CEA. Furthermore, there is little evidence to support the use of one form of monitoring over another in selecting patients requiring a shunt."10
As regards the method of monitoring in selective shunting, until the efficacy of shunting has been demonstrated, further trials of the method of monitoring are probably not merited."10 This Cochrane analysis does not address the use of other potential strategies for brain protection during endarterectomy such as hypothermia, burst suppression, or induced hypertension or techniques performed on an awake patient (either endovascular carotid angioplasty or transcutaneous endarterectomy performed under local anesthesia).
After one has made the decision to monitor EEG for cerebral ischemic changes during any surgery, one is then confronted with the problem of determining if a change in EEG is attributable to focal hypoperfusion, generalized hypoperfusion (from low systemic blood pressure), or anesthetic effect. These possibilities guide anesthesiologists toward a strategy of anesthetic management during procedures that may result in ischemia.
Rely on anesthetic agents that have the least effect on EEG activity (short-acting narcotics, benzodiazepine) (Table 33-3).
Maintain a constant anesthetic level throughout procedure, especially at critical periods.
Be prepared to raise and lower blood pressure with nonanesthetic agents (inotropes, chronotropes, vasoactive drugs, and volume).
Be prepared to use alternative ischemia monitors (ie, somatosensory evoked potential [SSEP] if burst suppression is to be used for "cerebral protection").
Perform the carotid surgery with the patient awake.
Table 33-3 Table of Intravenous and Inhalational Anesthetic Effect on Somatosensory Evoked Potential and Electroencephalography* ||Download (.pdf)
Table 33-3 Table of Intravenous and Inhalational Anesthetic Effect on Somatosensory Evoked Potential and Electroencephalography*
|Early Cortical Waveform§|
Using Electroencephalography to Monitor Burst Suppression
The human data regarding burst suppression as a guide to administration of anesthetics for cerebral protection are mixed. Patients in whom focal iatrogenic ischemia is induced during middle cerebral artery (MCA) aneurysm clip ligation have a significant advantage over those receiving isoflurane when they are given pentobarbital as the primary neuroprotective agent or when they receive propofol or etomidate titrated to achieve EEG burst suppression.11 Melgar et al12 propose the use of EEG to identify CEA patients who develop ischemic changes following carotid cross clamp that are refractory to induced hypertension. To these patients, these authors administer etomidate to achieve burst suppression and proceed with endarterectomy without shunting. Bush et al13 conclude: "Percutaneous carotid stenting with neuroprotection provides comparable clinical success to CEA performed under local anesthetic."
However, a multicenter study of the protective effects of propofol-induced burst suppression during cardiac valve replacement showed no effect.14 Burst suppression achieved through various means (barbiturate or isoflurane) resulted in different effects on cerebral blood flow and calculated cerebral requirement for oxygen,15 demonstrating that the balance of oxygen delivery to consumption is altered differently by these 2 agents at equivalent degrees of burst suppression. Therefore, the use of burst suppression as a guide to anesthetic administration during procedures that place the cortex at risk must take account of the anesthetic agent used for the burst suppression, the surgical procedure for which it is intended, and the other hemodynamic and ventilatory parameters effecting oxygen delivery to the cortex.