Invasive recording techniques, in which electrodes are placed on or in the brain to record its activity, are important electrophysiologic tools in the presurgical evaluation and surgical treatment of patients with epilepsy. Similarly, intraoperative microelectrode recordings obtained from deep brain structures are valuable in guiding the surgical treatment of patients with movement disorders, particularly Parkinson disease, essential tremor, and dystonia.
Invasive techniques in epilepsy
Epilepsy Surgery and Localization of the Epileptogenic Zone
The pioneering work in the 1930s of Penfield and colleagues at the Montreal Neurological Institute established the effectiveness of surgical treatment in controlling seizures in some epileptic patients who do not respond adequately to medical therapy. Despite the wide range of medical treatments for epilepsy currently available, approximately 30 to 35 percent of persons with epilepsy continue to experience seizures. For these patients with medically refractory epilepsy, surgical removal of the epileptogenic brain tissue is often an effective treatment. Surgical resection is predicated on the ability to identify the seizure focus or epileptogenic zone. This area of the brain is responsible for the generation of seizures, and its removal or disconnection results in the cessation of seizures. Techniques for identifying the seizure focus are continually evolving and being refined. Although a number of components typically constitute the contemporary presurgical evaluation of patients with medically refractory epilepsy, ictal electrophysiology remains the “gold standard” in this endeavor. When the scalp-recorded electroencephalogram (EEG) fails to provide adequate electrophysiologic localization of the epileptogenic region, or when it suggests localization that conflicts with the findings from other elements of the preoperative evaluation (e.g., neuroimaging), invasive recordings are necessary to identify clearly the brain region from which seizures arise.
Role and Limitations of Surface EEG in Evaluating Patients with Epilepsy
The ability to record the electrophysiologic activity of the brain with the use of surface electrodes applied to the scalp is rather remarkable when one considers the relatively low amplitude of the signal compared with other biologic signals and with environmental noise, the attenuating effects of tissues intervening between brain and scalp, and the distance between surface electrodes and cerebral generators. Without question, the surface EEG is indispensable in the evaluation of epileptic patients. Its utility includes detection of interictal epileptiform activity, strengthening a suspected diagnosis of epilepsy; identification of focal abnormalities, suggesting a focal structural brain lesion as a possible basis for seizures; and documentation of specific epileptiform patterns associated with particular epilepsy syndromes.
The ictal EEG (i.e., the EEG recorded during a seizure) is especially important in defining the epileptogenic focus in patients with epilepsies producing focal seizures (referred to in past classification schemes as localization-related or partial epilepsy). Long-term recordings of the scalp EEG combined with simultaneous video recordings of clinical behaviors during seizures (video-EEG monitoring) are essential in the evaluation of patients being considered for surgical treatment. For patients to be good candidates for focal resective surgery (e.g., temporal lobectomy or frontal topectomy), their seizures must be localized electrophysiologically to one discrete brain region.
With current EEG technology, electrophysiologic seizure localization can often be accomplished with the scalp-recorded EEG; however, in approximately 30 percent of patients, the surface-recorded ictal EEG is inadequate for this purpose. At times, the surface EEG is simply not helpful in providing information of localizing value, whereas on other occasions it is misleading. For example, the EEG recordings may provide localizing but not lateralizing information, as when simultaneous bitemporal seizure onsets are found ( Fig. 7-1 ). Similarly, the EEG may lateralize the seizure focus to the right or left hemisphere, but may not localize the epileptogenic zone to a particular region. Furthermore, the EEG can be misleading, reflecting activity predominantly in areas to which the seizure has spread and not the area from which it has arisen. To minimize this risk, the EEG findings localizing the seizure focus must begin with or precede the behavioral onset of the seizure as documented by the video recordings.
Role of Invasive Recordings in Evaluating Patients with Epilepsy
In patients with medically refractory epilepsy who are being considered for surgical treatment, invasive recording techniques are used in situations in which the surface EEG (recorded with scalp and sphenoidal electrodes) does not provide adequate localization of the epileptogenic focus or provides discordant localization in relation to other studies. These invasive techniques involve the surgical placement of intracranial electrodes in the subdural or epidural spaces or within the brain parenchyma ( Fig. 7-2 ). No consensus exists among experienced epileptologists concerning the specific indications for one technique rather than another. Regardless of the technique, the rationale is to place recording electrodes close to brain regions thought to be generating seizures in order to identify the epileptogenic region with certainty. In addition to their role in recording the electrical activity of the brain, arrays of electrodes contained on a grid can be located atop the cortical surface and used for mapping studies. These studies use cortical stimulation to identify areas of functional importance that are to be avoided in the surgical resection.
Invasive electrodes, when properly located, provide the obvious advantage of recording seizure activity directly from, or close to, its source. Nevertheless, for practical reasons, the extent of brain area sampled by invasive electrodes is limited, and therefore the ability to survey widespread areas of the brain (accomplished well by the scalp-recorded EEG) is sacrificed to varying degrees in invasive recordings. If invasive electrodes are not near the site of seizure origin, the recordings obtained may be misleading. Thus, the type of electrodes used and the areas in which they are placed in a particular patient are of critical importance. The placement of invasive electrodes is guided by the scalp ictal and interictal EEG, as well as by other studies, such as magnetic resonance imaging (MRI), single photon emission computed tomography (SPECT), and positron emission tomography (PET). Abnormalities identified on high-resolution MRI, especially the features that suggest the structural substrate of the epileptogenic region, provide important information for guiding the placement of invasive electrodes ( Fig. 7-3 ). Other components of the evaluation that may be helpful in directing intracranial electrodes to brain regions likely to yield reliable localizing information include abnormalities identified on neurologic examination, the ictal clinical features (clinical behaviors and signs during the seizure, as discussed in Chapter 6 ), and abnormalities revealed on functional imaging studies, including PET, SPECT, and magnetic resonance spectroscopy (MRS). These factors must also be considered when one interprets the recordings provided by invasive electrodes.
Because invasive recording techniques, though generally safe, are associated with potential morbidity, they are reserved for patients who desire operative treatment and in whom surgery is considered appropriate. These approaches are necessary when adequate localizing information cannot be obtained by noninvasive methods. Specific intracranial recording techniques are considered in the following sections.
Depth electroencephalography
Definition and Indications
Depth electrodes allow the direct recording of cerebral activity from the brain parenchyma into which they are implanted. The indications for depth electrode recordings are not agreed universally, but the method is particularly well suited to investigating seizures suspected of arising from deep structures such as the hippocampus, amygdala, and medial frontal lobe. Seizures arising from these areas may be difficult to localize with surface recordings because of the closed electric fields and attenuation of the activity by the time it arrives, if at all, at superficial electrode sites. Furthermore, rapid transit of seizures to homologous contralateral regions sometimes precludes the ability to lateralize the area of onset of seizures, even with subdural electrode strips. For example, seizures originating from one hippocampus often spread quickly to the opposite hippocampus, with scalp-sphenoidal or subdural recordings commonly reflecting an apparent synchronous onset of the seizure from both temporal regions. Depth electrodes, because of their unique ability to record seizure activity directly from the hippocampus, are often useful in establishing the hippocampus from which the seizures arise. In addition, the presence of bilateral, independent epileptogenic foci—not always obvious from surface recordings—can often be demonstrated with depth recordings.
Techniques
Rigid and flexible electrodes constructed of a variety of metals and containing a variable number of contacts have been used for chronic depth recordings; the recent availability of electrodes constructed of nonmagnetic materials has allowed postimplantation imaging with MRI to document the anatomic location of the electrodes. Modern placement of depth electrodes utilizing MRI- or computed tomography (CT)-guided stereotactic techniques allows accurate and safe implantation of the electrodes through cranial burr holes with the patient under local or general anesthesia. The trajectory of electrode implantation depends on the location of the suspected epileptogenic focus and on the customary practices at the center where the study is to be undertaken.
Two common depth electrode arrangements are employed to study temporal lobe epilepsy: (1) an orthogonal approach in the horizontal plane, in which three electrodes are implanted on each side through the middle temporal gyrus, with the most distal contacts inserted into the amygdala, anterior hippocampus, and posterior hippocampus; and (2) a longitudinal approach, in which a single electrode is inserted through an occipital burr hole on each side and traverses the long axis of the hippocampus. The orthogonal technique offers the advantage of recording from both the medial and the lateral aspects along the temporal lobe but, compared with the longitudinal approach, requires a greater number of electrodes to do so.
Findings
The interpretation of depth recordings, as with all intracranial recordings, differs from that of surface EEG recordings. First, the electrode is in close proximity to the source of activity, and so the amplitude of the signal is relatively high. Various components of the signal (especially high-frequency activity) are therefore more robust than those recorded with surface electrodes. Second, depth electrodes record activity from a spatially restricted field.
The relevance of background abnormalities recorded by depth electrodes is not clear. Slow-wave disturbances and attenuation of background rhythms may be seen. Such findings do not necessarily correspond to the epileptogenic zone and may represent injury potentials secondary to electrode insertion. In addition, normal background activity is commonly quite sharp in configuration and may assume a rhythmic appearance. Interictal epileptiform abnormalities recorded by depth electrodes are typically of steeper slope, higher amplitude, and briefer duration than those recorded with surface electrodes. The frequency of bitemporal spikes and sharp waves in patients with unilateral temporal lobe epilepsy (defined by ictal depth recordings) is substantially higher in depth recordings than that found in scalp EEG recordings. Ictal patterns recorded at seizure onset with depth electrodes in temporal lobe epilepsy include attenuation of background activity; repetitive, sharp slow waves; rhythmic discharges of beta, alpha, or theta frequency; and irregular slow or sharp waves ( Fig. 7-4 ). In temporal lobe seizures, intraparenchymal recordings commonly demonstrate electrographic onset of the ictus earlier than do subdural recordings. Auras (simple partial seizures), although typically not associated with ictal patterns on scalp recordings, often correlate with electrocerebral changes that are detected by implanted electrodes. Similarly, subclinical seizures are detected more commonly by depth recordings. Focal seizure onsets, in which electrographic changes begin at one or two adjacent contacts of the depth electrode, most commonly are recorded from the hippocampus, but regional onsets may also be seen. Less often, seizures originate in a focal manner from the amygdala. In the absence of a lesion, seizures rarely are seen to arise from the lateral temporal neocortex.
Advantages, Limitations, and Complications
Depth electrode recordings from brain parenchyma provide a sensitive means of recording, with negligible artifact, activity occurring in a limited volume of brain in the vicinity of the electrode. Although the sensitivity and clarity of the signal are heightened with depth recordings, the constricted “field of view” inherent in all intracranial techniques results in the risk that the recorded activity originated from afar and propagated to a brain region sampled by the implanted electrode. Thus interpretation of depth recordings must be performed within the larger context of data provided from other aspects of the evaluation.
Morbidity complicating the use of depth electrodes includes hemorrhage and infection. The risk of hemorrhage is estimated to be less than 2 percent but may result in permanent neurologic sequelae or even death. Most infections respond to antibiotic treatment.
Subdural strip electrode recordings
Definition and Indications
Subdural strip electrodes consist of a matrix of flexible material in which electrode contacts, arranged in a single row at fixed interelectrode distances (typically 10 mm), are embedded. Each strip is inserted under the dura through a cranial burr hole and directed to overlie the cortical surface of interest. This method is used most commonly to ascertain the localization and lateralization of an epileptogenic focus in a patient whose surface recordings fail to provide this information. Although subdural electrode recordings have been used in the evaluation of the epileptic brain since the 1930s, the technique gained more routine use in the United States in the early 1980s, when experience indicated that the relatively less invasive subdural approach often supplanted the need for the more invasive depth electrode techniques.
Placement of multiple subdural electrode strips is undertaken typically to survey several cortical regions bilaterally. For example, in patients suspected of having a temporal lobe focus, subdural strips can be inserted through a temporal burr hole and directed laterally and subtemporally on either side to record from neocortical and mediobasal structures, respectively. Additional electrode strips are often placed through a frontal burr hole to record from the dorsolateral or opercular frontal regions; seizures may arise from these areas and spread to temporal regions, with clinical seizure symptomatology and the surface EEG erroneously suggesting temporal lobe onset.
Subdural strip electrodes are also useful in the clarification of whether the epileptogenic region is associated with a lesion evident on MRI when scalp recordings are discordant with the imaging findings. For example, the scalp-recorded EEG tracings depicted in Figure 7-5, A are from a patient with medically refractory complex partial seizures whose MRI is shown in Figure 7-5, B . These surface recordings suggested that seizures were arising from the left temporal lobe, whereas the MRI revealed a lesion in the right anterior temporal lobe consistent with a cavernous angioma. Because cavernous angiomas are often implicated in an epileptogenic region, the surface EEG localization was questioned and subdural strip electrodes therefore were implanted in both subtemporal regions. Ictal recordings with these electrodes demonstrated that, indeed, the patient’s seizures did originate from the area of the lesion ( Fig. 7-5, C ). Resection of the lesion and the immediately adjacent cortex resulted in cessation of the patient’s seizures.
The presence of a lesion on MRI does not necessarily imply that it is the site of seizure origination, however, because lesions identified on neuroimaging may be incidental and not related to the epileptogenic region. Further complicating the presurgical evaluation, some patients demonstrate multiple areas of abnormality on imaging (e.g., multiple areas of post-traumatic encephalomalacia, vascular malformations, and areas of cortical malformation); one, some, or none of these areas may be epileptogenic.
Techniques
Strip electrodes are available in a variety of lengths and widths, and with various numbers of contacts and interelectrode spacings. Six-contact strips are often used routinely, although longer or shorter arrays may be employed depending on the locations in which they are to be placed. Strip electrodes are implanted surgically through cranial burr holes, usually with the patient under general anesthesia; multiple strips, directed at different regions, may be inserted through a single burr hole or through multiple burr holes bilaterally. The electrodes typically are placed under fluoroscopic guidance to ensure delivery to the region of interest. Commonly, burr holes are made superior to the zygoma and slightly anterior to the ear for the placement of electrodes in the subtemporal and lateral temporal regions. Strips also can be directed posteriorly to record from the occipital regions, if indicated. Frontal burr holes, located 4 to 6 cm anterior to the coronal suture and slightly lateral to the midline, allow subdural placement of strips along the interhemispheric fissure, to record from medial frontal areas; and across the lateral frontal region, to record from dorsolateral frontal and orbitofrontal regions. With the use of methods similar to those for depth electrodes, the cables from each electrode exit through stab wounds separate from those associated with the burr hole; such an arrangement helps to anchor each strip and reduces cerebrospinal fluid leaks and infection. Skull X-ray, CT, or MRI allows verification of electrode location in relation to the anatomic target.
Both referential and bipolar montages are employed to interpret subdural strip recordings. A scalp electrode can serve as a convenient reference; because of the voltage difference between the scalp and the brain surface, the scalp reference is rarely active but can introduce electromyographic artifact into the recording.
Findings
The interpretation of subdural strip recordings, as with depth electrode recordings, must take into consideration the somewhat restricted sampling of brain activity provided by the technique. Recording from homologous contacts of bilateral strips assists in the assessment of background activity, aids in differentiating localized or lateralized changes in the EEG (or more precisely, the electrocorticogram [ECoG]), and enables a better understanding of seizure propagation patterns.
As with depth recordings, localized disturbances of background rhythms may be seen and do not necessarily correspond to the epileptogenic region. Interictal epileptiform discharges are detected more commonly with subdural than with surface recordings, whereas the frequencies of spikes recorded with subdural and depth recordings are similar. Ictal patterns consist of a distinct alteration of background activity. Similar to depth recordings, electrographic seizure onsets recorded with subdural strips may assume several morphologies, including the abrupt onset of rhythmic spike or sharp-wave activity, low-voltage fast activity, or suppression of background activity (see Fig. 7-5, C ).
Several series comparing subdural and depth electrode recordings in epilepsy syndromes producing focal seizures (mainly of temporal lobe origin) have been published. These reports generally conclude that inferior temporal subdural strip electrodes are somewhat less sensitive than depth electrodes (80 percent compared with 100 percent, respectively) in localizing seizures of medial temporal lobe onset. Importantly, though, the 20 percent of seizures not localized by subdural recordings were not falsely localized; their recordings simply were not localized at all. Thus, a case can be made for subdural recordings as the next phase in evaluating patients with suspected temporal lobe epilepsy where scalp recordings are nonlocalizing. Such recordings are reasonably sensitive, can cover a larger region of brain than depth electrodes, typically are not misleading, and are less invasive and therefore less likely to cause morbidity or mortality compared with depth electrodes. For the minority of patients with temporal lobe epilepsy in whom subdural recordings are also nonlocalizing, depth recordings may then be undertaken. Many epileptologists employ this graduated approach to invasive studies, especially for patients in whom other studies (e.g., MRI or PET) suggest localization.
Subdural recording techniques are valuable in the evaluation of extratemporal lobe epilepsy. Although depth electrodes can be utilized, the large area of cortical surface to be assessed limits their utility. Even in patients with mediofrontal or orbitofrontal epilepsy, subdural electrodes may be superior to depth electrodes in that they cover larger cortical areas, do not need to traverse long distances of brain uninvolved in seizure generation (i.e., white matter), and provide the capacity to record from a greater cortical volume at each contact. In certain clinical situations, the data provided by subdural and depth electrode recordings are complementary, and their contemporaneous use may be considered.
Advantages, Limitations, and Complications
The technique of recording with multiple subdural strip electrodes offers the advantage of acquiring ictal recordings directly from the cortical surface at many locations in a minimally invasive and relatively safe manner. Compared with depth electrodes, subdural strips are easier to implant as well, because stereotactic procedures are not required. Like other invasive techniques, subdural strip recordings provide a limited sample of cerebral activity. If the electrodes are not placed near the epileptogenic region, recordings may be nonlocalizing or even misleading, detecting propagated activity rather than activity representing the onset of the ictus. As discussed earlier, even when strips are placed subtemporally along the inferior temporal lobe, the subdural recordings may fail to localize hippocampal seizure onsets.
Of all the invasive, extraoperative techniques used for evaluating epilepsy, subdural strip electrodes carry the lowest morbidity rate (less than 1 percent). Infection accounts for the majority of complications and typically is eradicated readily with antibiotics. Other reported complications, which are rare with subdural strips, include unintended extraction of the electrodes by patients in the peri-ictal period (a potential complication of any invasive recording procedure), subdural empyema, and cortical contusion. No mortality has been reported with the technique.
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