Preoperative Planning

Magnetic resonance imaging (MRI) has been extremely helpful in predicting the relationship of motor cortex to a tumor by identifying a few constant MRI landmarks. On T2-weighted axial images near the convexity, a pair of mirror-image lines nearly perpendicular to the falx may be readily identified and represent the central sulcus.^5,6 Large lesions may compress the sulcus and distort the regional anatomy, but the landmark is usually identified by comparing the hemispheres on T1- and T2-weighted images. Although less sensitive, a midline sagittal image and a lateral parasagittal image may be viewed with respect to the marginal ramus of the cingulate sulcus and a perpendicular line drawn from the posterior roof of the insular triangle to identify the rolandic cortex.

The anterior suprasylvian region can have varying sulcus topography, and a classification based on anatomic landmarks has been published by Ebeling and coworkers.⁷ Correlation has been shown between the structure of the frontal operculum as seen on MRI and the location of Broca’s area, which allows preoperative prediction of this location.⁸

Patients with dense hemiparesis are not good candidates for mapping the motor pathways intraoperatively regardless of the stimulation used. Volitional movements of the face and extremities may be stimulated by cortical and subcortical mapping intraoperatively, but children younger than 5 to 7 years often have an electrically inexcitable cortex when a direct stimulating current is applied with a bipolar electrode.^9,10 Complex stimulating paradigms may still, however, bring out the excitability of pediatric motor cortex.¹¹ With the use of somatosensory evoked potentials (SSEPs), phase reversal over the central sulcus is available if direct stimulation mapping cannot be accomplished easily.^12–15 Insertion of a subdural electrode array under general anesthesia followed by extraoperative mapping may allow the mapping of motor, sensory, language, and ictal seizure onsets in children before early adolescence and in uncooperative adults. These techniques may be contraindicated in those with significant cerebral edema from malignant gliomas or metastatic tumors and may expose patients to a second craniotomy with its inherent risk of poor contact with the cortical surface as a result of blood or cerebrospinal fluid collecting underneath the electrodes. Delayed infection is also possible.¹⁶

Foundations of Language Mapping in Epilepsy Surgery

Stimulation mapping during language measurement in awake adults has shown several features of the cortical organization of language that are not anticipated from the effect of brain lesions.¹⁷

Several of these features are of major importance in planning dominant hemisphere resections, including the high degree of localization of sites with repeated evoked errors in one language measure (and thus essential for function), but with broad variance across the patient population in terms of the exact locations of these sites. In a series of 117 patients undergoing intraoperative stimulation mapping in the left dominant perisylvian cortex during naming, Ojemann and colleagues found that most patients had essential sites with surface areas of 2 cm or less, with only 16% having an area of essential language sites as large as 6 cm.¹⁸ It has been shown that if another language is acquired as a second language, more diffuse localization is seen than with the primary language (Haglund and Ojemann, unpublished observations). It has also been shown in sign language patients that localization of American sign language differs slightly from that of naming in hearing patients proficient in sign language.¹⁹ The discrete localization is evident in both the frontal and temporoparietal sites and has been demonstrated with naming and word and sentence reading as language measures. Some sites have very sharp boundaries, whereas others have a surrounding area in which occasional errors are evoked, thus suggesting a more graded transition from cortex unrelated to language to that essential for it.^20,21

In most patients, several essential perisylvian areas are involved in language function. In a series of 117 patients, two thirds had two sites; in a quarter, three sites were present. Usually, there was one frontal site and one or more temporoparietal sites; however, in approximately 10% of patients there was no frontal language site, and around another 10% had no temporoparietal language site. Although a majority of patients have temporoparietal language sites, the critical issue here is the large variance between patients.

The considerable variance in language localization is illustrated in Figure 57-1. The percentage of essential language sites in the entire series is shown in the circles and demonstrates a range in the temporoparietal region of 2% to 36% of patients with essential language sites in a single area. Note the 14% of essential language sites in the anterior superior temporal gyrus and 5% of such sites in the anterior middle temporal gyrus, in front of the central sulcus. In the posterior language area, no local area was crucial for language in more than about a third of the patients. This variation in language localization is substantially greater than the morphologic variability in the perisylvian cortex, although this is also substantial.^22,23 However, no cytoarchitectonic area seems to have a reliable relationship to language. It is the combination of discrete localization of essential language areas in the individual patient and the great variation in their location across the population that form the basis for using stimulation mapping rather than anatomic landmarks in planning resection near eloquent cortex.

FIGURE 57-1 Localization of cortical sites essential for language (object naming) was assessed by stimulation mapping in the left, dominant hemispheres of 117 patients. Sites were related to language when stimulation at a current below the threshold for afterdischarge evoked repeated statistically significant errors in object naming. Small numbers above the circles indicate the number of patients who were tested at a site, and the number within the circle indicates the percentage of tested patients who were found to have a language site at this location.

(Adapted from Ojemann G, Ojemann J, Lettich E, et al. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg. 1989;71:316.)

Stimulation mapping in children has shown a lower frequency of sites of stimulation-induced errors than in the adult population.²⁴ This finding implies that new language areas may still arise with maturation in children during the age range of 4 through 16 years. In children younger than 10 years, language cortex is less likely to be identified by stimulation mapping than in older children. Wada testing seems to be more likely to be successful than stimulation mapping in this younger age group.²⁵ Extraoperative electrocortical stimulation mapping, however, is an established procedure for surgery near eloquent cortex in children.²⁶ Because awake craniotomy is less tolerable for children, implantation of subdural stimulation electrodes allows precise extraoperative mapping of cortical function without psychological trauma.

Anatomic knowledge of subcortical white matter tract connectivity in the temporal lobe is important for preventing postoperative deficits. The uncinate fasciculus connects the uncus, amygdala, and hippocampal gyrus to the orbital and frontopolar cortex.²⁷ No functional role has yet been attributed to the uncinate fasciculus, and resection of it is performed routinely in epilepsy surgery.

The inferior longitudinal fasciculus connects the anterior part of the temporal lobe to the occipital pole and has also been shown to play no role in language processing.²⁸ The inferior occipitofrontal fasciculus runs from the occipital lobe laterally to the lateral wall of the temporal horn of the lateral ventricle and then continues through the external capsule to the orbitofrontal and dorsolateral prefrontal cortices. Direct stimulation of this pathway induces semantic paraphasias,²⁹ so care should be taken to not disrupt this pathway during surgery. The superior longitudinal fasciculus is also called the arcuate fasciculus and connects Wernicke’s area in the posterior and superior temporal cortex with Broca’s area in the frontal lobe. Preservation of this pathway during surgery is mandatory because section of it produces phonemic paraphasias.³⁰ Finally, it is important to preserve the optical pathways to prevent the development of permanent postoperative hemianopia. Intraoperative stimulation mapping can elicit a transient shadow that can be used to identify the visual pathways.³¹

Assessment of the effects of stimulation on an array of language-related functions (naming, reading, recent verbal memory, orofacial mimicry, and speech sound identification) in a series of 14 patients provided the basis for a model of language organization in the lateral perisylvian cortex. This model included a perisylvian area involving the superior temporal and anterior parietal as well as the posterior frontal lobes important for speech production and perception, a surrounding zone of specialized sites, some of which are related to syntax, and an even more peripheral area related to recent verbal memory.^32,33 Significant interference with reading has been noted with stimulation of the lower part of the precentral and postcentral gyri; the dominant supramarginal, angular, and posterior part of the superior temporal gyri; the dominant inferior and middle frontal gyri; and the posterior part of the dominant middle temporal gyrus.³⁴

Positive language sites in bilingual patients may or may not colocalize. In an individual who acquired both languages during infancy, anomia was demonstrated for both languages when stimulation was performed at the same sites.³⁵ Four patients who acquired their second language during early school years (5 or 6 years of age) exhibited varying degrees of anomia in the second language.

Different tasks such as naming, reading, and responding may share the same cortical site, in which case they are referred to as multiuse sites.³⁶ Multimodality language mapping can generate an accurate map of eloquent language cortex in bilingual patients. Single-task sites are defined as sites where one task is disrupted across both languages with stimulation. Single-use sites are sites where one task is disrupted in only one language with stimulation. Cortical mapping of a bilingual patient has shown the presence of multiuse, single-task, and single-use sites, which underlines the necessity to test for both different languages and different language modalities if optimal postoperative functional outcomes are to be achieved.³⁷

Many neurosurgical operating teams rely solely on visual naming tasks for the intraoperative testing of language function. Resection of auditory naming sites has, however, been shown to lead to postoperative word-finding difficulties.³⁸ Preservation of auditory naming and reading sites is critical for preserving language function, and intraoperative removal of these sites may account for up to 25% of the language deficits seen postoperatively.³⁹ Figure 57-2 illustrates that there are distinct as well as overlapping language sites that can be identified during intraoperative stimulation mapping for visual naming, auditory naming, reading, and word finding.

FIGURE 57-2 The human brain contains distinct as well as overlapping sites for visual naming, auditory naming, and sentence completion. This figure shows one example of intraoperative mapping results. Blue boxes represent visual naming sites; yellow boxes, auditory naming sites; and white letters, sites crucial for sentence completion (R, reading; W, word finding). Green boxes illustrate overlapping sites for visual naming, auditory naming, and sentence completion. Light yellow boxes mark sites that are shared by auditory naming and sentence completion only. Numbers 1 and 2 are placed on the face motor cortex and numbers 3 and 4 on the face sensory cortex.

The extent of separation of language-related functions and the relationships of areas to one another constitute an active area of research in stimulation mapping techniques and single-unit microelectrode recordings.^40–43

The Wada Test

In their original article in 1960, Juhn Wada and Theodore Rasmussen at the Montreal Neurological Institute described an invasive procedure for the lateralization of speech that has become to be known as the Wada test.⁴⁴ The procedure involves the injection of 150 to 200 mg of amobarbital (Amytal) sodium into the common carotid artery. An angiogram should be performed before the injection to rule out persistent trigeminal, otic, hypoglossal, or proatlantic arteries and avoid respiratory or circulatory problems as a result of shunting of the injection solution to the brainstem. The injection is made with the patient counting, the forearms up in the air, and the fingers either moving constantly or gripping an examiner’s hands. As the injection is completed, the contralateral arm will become hemiplegic and flaccid. The patient is usually hesitant in counting on the dominant and nondominant side toward the end of the injection but then is quickly able to resume counting and naming objects while the contralateral hemiplegia still persists if the nondominant hemisphere is injected. In the case of injection into the dominant hemisphere, the patient is unable to continue counting or naming objects while the contralateral hemiplegia is complete. The patient is still able to follow commands, although on the side ipsilateral to the injection, which is tested to ensure that the aphasia is not due to confusion. At doses of 150 to 200 mg of Amytal Sodium, the contralateral hemiplegia typically lasts 1.5 to 5 minutes. Thirty to 90 seconds after the contralateral hemiplegia begins to resolve, the patient regains the ability to answer questions requiring yes and no answers. This is followed by a period of dysphasia that typically lasts for 1 to 3 minutes until normal speech is restored.

Although the Wada test has proved to be an important tool in the presurgical evaluation of epilepsy surgery patients for more than 50 years, it has lost some of its clinical significance over recent years with the advent of newer imaging techniques.⁴⁵ The majority of epilepsy centers no longer conduct a Wada test on every surgical candidate. In one multicenter study, 50% of respondents stated that they used the Wada test for less than 25% of their surgical epilepsy patients.⁴⁶ Functional MRI has largely replaced the Wada test for language lateralization in the preoperative evaluation of epilepsy patients to answer the question of whether language mapping should be performed during the resection. Therefore, the Wada test is now used mostly to screen for a patient’s postoperative risk for memory deficits and amnesia. The indication for Wada testing in these cases may be limited to bilateral hippocampal pathology or epileptiform activity because one normal remaining hippocampus on fine-cut MRI scans after resection can usually sustain memory. The advent of MRI technology has further diminished the importance of Wada testing over the years since bilateral hippocampal anatomic abnormalities can now be studied with high-resolution coronal MRI.

Amnesia after unilateral anterior temporal lobe resection is a very rare occurrence.⁴⁷ Only about 20 patients have been reported in the literature.⁴⁸ In 3 of these patients, Wada testing had been performed before surgery and accurately predicted postoperative amnesia.^49–51 Therefore, surgical resection is often not performed on patients who fail the memory portion of the Wada test. However, one study involving 10 patients showed that all patients still retained memory after temporal lobe resections even if they failed the memory portion of the Wada test.⁵² Other investigators have also demonstrated that a failed memory portion of the Wada test does not predict an amnestic syndrome,⁵³ and many epilepsy centers repeat the Wada test until the patient passes. Thus, use of the Wada test to evaluate for postoperative amnesia is also controversial. Noninvasive neuropsychological tests have been shown to be accurate predictors of postoperative neurocognitive and memory decline, so the Wada test does not always need to be used for this assessment as well.^54,55

The Wada test is an invasive procedure with a reported complication rate of 0.5% to 10%.⁵⁶ Consequently, patients should be carefully selected on a case-by-case basis to determine the appropriateness of Wada testing. Many of the patients now undergoing Wada testing have disconcordant findings on video-electroencephalographic (EEG) recordings, high-resolution fine-cut hippocampal MRI, or neuropsychological testing. Furthermore, some clinicians have completely omitted Wada testing from their decision-making algorithms for epilepsy surgery.⁵⁷ Currently, the Wada test is used mostly to test for the ability to sustain memory in the setting of bilateral hippocampal pathology.

Noninvasive Brain Mapping

Functional MRI, positron emission tomography (PET), and magnetoencephalography (MEG) are noninvasive tools used to search for the location of eloquent cortex.^58,59 Functional MRI is based on measurement of the real-time increase in deoxyhemoglobin in the venous structures associated with motor movement, sensory perception, or speech generation.⁵⁸

The question is whether functional MRI as a noninvasive method can replace the Wada test in determining language lateralization. Although lesion and Wada studies have shown that only the left hemisphere is dominant in the majority of subjects, functional MRI typically demonstrates some degree of activity in the hemisphere contralateral to the Wada-dominant hemisphere in virtually all individuals. The language lateralization index is therefore used in functional MRI to determine hemispheric dominance. One method of calculating this index consists of defining an area of interest that has a known association with language function on MRI (Broca’s area, for example) and subsequently performing a simple bilateral suprathreshold count in the region of interest.⁶⁰ Reproducibility of the language lateralization index has, however, been found to strongly vary between task analyses. Object naming has been found to be a more sensitive measure of speech localization than has number counting.⁶¹ The language lateralization index showed significant correlation between sessions in the same individual for verb generation tasks, whereas no significant correlation was found for picture naming and only a weak correlation was seen in the antonym generation task.⁶² Therefore, only the verb generation task allows a reliable calculation of the lateralization index across sessions. When the verb generation task was used to determine hemispheric dominance, functional MRI was concordant with invasive measures (Wada testing or cortical stimulation) in all but 1 of 23 patients in one study.⁶³ Correlation of the results for language lateralization between functional MRI and Wada testing was found to be highly significant in another study.⁶⁴ Thus, functional MRI based on the verb generation task has replaced Wada testing at many institutions in the United States for the determination of language dominance.

The inability of functional MRI to currently produce reliable results across all language tasks has raised concern about its general applicability to intraoperative surgical planning in eloquent cortex. Such concern is due to the fact that functional MRI has been shown to miss cortical sites that are found to be essential by intraoperative stimulation mapping.⁶⁵ To analyze its sensitivity and specificity with respect to direct cortical mapping, functional MRI data were registered in a frameless stereotactic neuronavigational device and correlated with the results of direct brain mapping. Although the specificity of functional MRI has been shown to be high for naming and verb generation tasks,⁶⁶ poor sensitivity was noted (only 22% in naming tasks and 36% in verb generation tasks).⁶⁵ A combined battery of language tasks may enhance the sensitivity of functional MRI in comparison to testing individual language tasks.⁶⁷ The results, however, have discouraged the use of functional MRI as a tool for making critical surgical decisions in the absence of direct brain mapping. Functional MRI cannot replace stimulation mapping for positive language sites on the basis of the current state of technology.

Functional MRI has, however, been found to be a useful clinical tool for the prediction of selective motor cortex areas. Concordance between the contours of functional MRI and intraoperative electrical cortical mapping was found in 20 of 21 patients in one study that evaluated its reliability for the implantation of an epidural electrode for chronic motor cortex stimulation.⁶⁸

Functional cortex can also be mapped with PET. Speech eloquent areas can be localized with 2-[¹⁸F]-2-deoxy-D-glucose (FDG) based on the higher consumption of glucose in eloquent areas during verb generation tasks. Although integration of functional PET data into frameless navigation systems for surgical planning is possible, its low reliability has precluded it from replacing direct stimulation mapping as well. In three of seven patients, preoperative PET findings were not supported by intraoperative mapping.⁶⁹

In contrast to functional language areas, which vary in location between individuals, the primary motor cortex is always situated in the precentral gyrus. Pathology, however, can distort normal anatomy and make mapping procedures for cortical or subcortical motor structures essential to prevent a postoperative deficit.

In healthy individuals, MEG has been demonstrated to be capable of delineating the somatotopic organization of the motor cortex since its results were shown to correlate with anatomic landmarks.⁷⁰ Newer source reconstruction algorithms have increased its reliability in the clinical setting. In one patient with a perirolandic tumor, MEG correctly identified the hand motor area, which was subsequently confirmed by intraoperative cortical stimulation mapping.⁷¹ Somatosensory mapping with MEG can be used to guide intraoperative mapping of motor cortex. One study found a consistent quantitative relationship in the distance between the mouth motor cortex identified by electrical stimulation and the lip somatosensory cortex delineated by MEG.⁷² This relationship allows prediction of the location of the mouth motor cortex if the lip somatosensory cortex is detected by MEG. In one study including 15 patients, MEG depicted the central sulcus correctly in all patients and proved to be superior to functional MRI in localizing the somatosensory cortex.⁷³ MEG has also been shown to reliably map expressive and receptive language cortex.^74,75

The pyramidal tract is the major output source of fibers arising from the motor cortex. Diffusion-weighted imaging (DWI) and diffusion tensor imaging (DTI) are noninvasive techniques that allow preoperative visualization of the pyramidal tract on MRI.⁷⁶ The disadvantage of preoperative tractographic imaging lies in the possibility of an intraoperative shift of brain tissue secondary to opening of the dura or the administration of mannitol and dexamethasone (Decadron). Intraoperative DWI has therefore been developed to acquire more reliable data. Early experience in a small number of patients has shown that the accuracy and image quality of intraoperative DWI with an MRI scanner of low magnetic field strength (0.3 T) are sufficient for possible incorporation into an intraoperative neuronavigation system.⁷⁷

Bello and coworkers,⁷⁸ in contrast, were able to show that preoperatively performed motor and language DTI also allowed accurate intraoperative identification of eloquent fiber tracts through neuronavigation. They reported a sensitivity of 95% for detection of the corticospinal tract and 97% for language tracts, figures calculated by confirmation with intraoperative subcortical stimulation mapping. Another study consisting of nine patients found an average distance of 8.7 mm between positive stimulation sites and the preoperatively DTI-mapped fiber tracts and concluded that it can be used to define a safety margin around the tract.⁷⁹ Because DTI has only recently been added to intraoperative neuronavigational systems, further studies are needed to validate its reliability in the clinical setting.

Preoperative Testing