Edward F. Chang, Kunal P. Raygor and Mitchel S. Berger
Classic models of language organization posited that separate motor and sensory language foci existed in the inferior frontal gyrus (Broca's area) and superior temporal gyrus (Wernicke's area), respectively, and that connections between these sites (arcuate fasciculus) allowed for auditory-motor interaction. These theories have predominated for more than a century, but advances in neuroimaging and stimulation mapping have provided a more detailed description of the functional neuroanatomy of language. New insights have shaped modern network-based models of speech processing composed of parallel and interconnected streams involving both cortical and subcortical areas. Recent models emphasize processing in “dorsal” and “ventral” pathways, mediating phonological and semantic processing, respectively. Phonological processing occurs along a dorsal pathway, from the posterosuperior temporal to the inferior frontal cortices. On the other hand, semantic information is carried in a ventral pathway that runs from the temporal pole to the basal occipitotemporal cortex, with anterior connections. Functional MRI has poor positive predictive value in determining critical language sites and should only be used as an adjunct for preoperative planning. Cortical and subcortical mapping should be used to define functional resection boundaries in eloquent areas and remains the clinical gold standard. In tracing the historical advancements in our understanding of speech processing, the authors hope to not only provide practicing neurosurgeons with additional information that will aid in surgical planning and prevent postoperative morbidity, but also underscore the fact that neurosurgeons are in a unique position to further advance our understanding of the anatomy and functional organization of language.
Alfredo Quinones-Hinojosa, Edward F. Chang and Michael W. McDermott
Meningiomas arising from the falcotentorial junction are rare. As a result, their clinical presentation and surgical management are not well described. During the past 3 years, the authors have treated six patients with falcotentorial meningiomas.
Most patients presented with symptoms related to raised intracranial pressure, including headaches, papilledema, and visual and gait disturbances. Magnetic resonance imaging revealed a smooth, oval, or round mass, which was typically homogeneously enhancing. Angiography was useful in evaluating arterial supply for embolization, when possible, and determining the status of venous collateral supply and sinus patency. The authors detail the surgical technique used in all six patients. Postoperatively, patients experienced transient cortical blindness, which in all cases spontaneously resolved during the course of several days to weeks. They provide a comprehensive description of the presentation and surgical management of falcotentorial meningiomas.
An excellent outcome can be expected when surgery is predicated on detailed preoperative neuroimaging and knowledge of the nuances of the surgical technique.
Jonathan D. Breshears, Annette M. Molinaro and Edward F. Chang
The human ventral sensorimotor cortex (vSMC) is involved in facial expression, mastication, and swallowing, as well as the dynamic and highly coordinated movements of human speech production. However, vSMC organization remains poorly understood, and previously published population-driven maps of its somatotopy do not accurately reflect the variability across individuals in a quantitative, probabilistic fashion. The goal of this study was to describe the responses to electrical stimulation of the vSMC, generate probabilistic maps of function in the vSMC, and quantify the variability across individuals.
Photographic, video, and stereotactic MRI data of intraoperative electrical stimulation of the vSMC were collected for 33 patients undergoing awake craniotomy. Stimulation sites were converted to a 2D coordinate system based on anatomical landmarks. Motor, sensory, and speech stimulation responses were reviewed and classified. Probabilistic maps of stimulation responses were generated, and spatial variance was quantified.
In 33 patients, the authors identified 194 motor, 212 sensory, 61 speech-arrest, and 27 mixed responses. Responses were complex, stereotyped, and mostly nonphysiological movements, involving hand, orofacial, and laryngeal musculature. Within individuals, the presence of oral movement representations varied; however, the dorsal-ventral order was always preserved. The most robust motor responses were jaw (probability 0.85), tongue (0.64), lips (0.58), and throat (0.52). Vocalizations were seen in 6 patients (0.18), more dorsally near lip and dorsal throat areas. Sensory responses were spatially dispersed; however, patients' subjective reports were highly precise in localization within the mouth. The most robust responses included tongue (0.82) and lips (0.42). The probability of speech arrest was 0.85, highest 15–20 mm anterior to the central sulcus and just dorsal to the sylvian fissure, in the anterior precentral gyrus or pars opercularis.
The authors report probabilistic maps of function in the human vSMC based on intraoperative cortical electrical stimulation. These results define the expected range of mapping outcomes in the vSMC of a single individual and shed light on the functional organization of the vSMC supporting speech motor control and nonspeech functions.
Dario J. Englot, Edward F. Chang and Kurtis I. Auguste
Vagus nerve stimulation (VNS) was approved by the US FDA in 1997 as an adjunctive treatment for medically refractory epilepsy. It is considered for use in patients who are poor candidates for resection or those in whom resection has failed. However, disagreement regarding the utility of VNS in epilepsy continues because of the variability in benefit reported across clinical studies. Moreover, although VNS was approved only for adults and adolescents with partial epilepsy, its efficacy in children and in patients with generalized epilepsy remains unclear. The authors performed the first meta-analysis of VNS efficacy in epilepsy, identifying 74 clinical studies with 3321 patients suffering from intractable epilepsy. These studies included 3 blinded, randomized controlled trials (Class I evidence); 2 nonblinded, randomized controlled trials (Class II evidence); 10 prospective studies (Class III evidence); and numerous retrospective studies. After VNS, seizure frequency was reduced by an average of 45%, with a 36% reduction in seizures at 3–12 months after surgery and a 51% reduction after > 1 year of therapy. At the last follow-up, seizures were reduced by 50% or more in approximately 50% of the patients, and VNS predicted a ≥ 50% reduction in seizures with a main effects OR of 1.83 (95% CI 1.80–1.86). Patients with generalized epilepsy and children benefited significantly from VNS despite their exclusion from initial approval of the device. Furthermore, posttraumatic epilepsy and tuberous sclerosis were positive predictors of a favorable outcome. In conclusion, VNS is an effective and relatively safe adjunctive therapy in patients with medically refractory epilepsy not amenable to resection. However, it is important to recognize that complete seizure freedom is rarely achieved using VNS and that a quarter of patients do not receive any benefit from therapy.
Vincent Y. Wang, Edward F. Chang and Nicholas M. Barbaro
Focal cortical dysplasia (FCD) is found in approximately one-half of patients with medically refractory epilepsy. These lesions may involve only mild disorganization of the cortex, but they may also contain abnormal neuronal elements such as balloon cells. Advances in neuroimaging have allowed better identification of these lesions, and thus more patients have become surgical candidates. Molecular biology techniques have been used to explore the genetics and pathophysiological characteristics of FCD. Data from surgical series have shown that surgery often results in significant reduction or cessation of seizures, especially if the entire lesion is resected.
John H. Sampson
Dario J. Englot, Jonathan D. Breshears, Peter P. Sun, Edward F. Chang and Kurtis I. Auguste
While temporal lobe epilepsy (TLE) is the most common epilepsy syndrome in adults, seizures in children are more often extratemporal in origin. Extra–temporal lobe epilepsy (ETLE) in pediatric patients is often medically refractory, leading to significantly diminished quality of life. Seizure outcomes after resective surgery for pediatric ETLE vary tremendously in the literature, given diverse patient and epilepsy characteristics and small sample sizes. The authors performed a systematic review and meta-analysis of studies including 10 or more pediatric patients (age ≤ 19 years) published over the last 20 years examining seizure outcomes after resective surgery for ETLE, excluding hemispherectomy. Thirty-six studies were examined. These 36 studies included 1259 pediatric patients who underwent resective surgery for ETLE. Seizure freedom (Engel Class I outcome) was achieved in 704 (56%) of these 1259 patients postoperatively, and 555 patients (44%) continued to have seizures (Engel Class II–IV outcome). Shorter epilepsy duration (≤ 7 years, the median value in this study) was more predictive of seizure freedom than longer (> 7 years) seizure history (odds ratio [OR] 1.52, 95% confidence interval [CI] 1.07–2.14), suggesting that earlier intervention may be beneficial. Also, lesional epilepsy was associated with better seizure outcomes than nonlesional epilepsy (OR 1.34, 95% CI 1.19–1.49). Other predictors of seizure freedom included an absence of generalized seizures (OR 1.61, 95% CI 1.18–2.35) and localizing ictal electroencephalographic findings (OR 1.55, 95% CI 1.24–1.93). In conclusion, seizure outcomes after resective surgery for pediatric ETLE are less favorable than those associated with temporal lobectomy, but seizure freedom may be more common with earlier intervention and lesional epilepsy etiology. Children with continued debilitating seizures despite failure of multiple medication trials should be referred to a comprehensive pediatric epilepsy center for further medical and surgical evaluation.
Dario J. Englot, Seunggu J. Han, Michael T. Lawton and Edward F. Chang
Seizures are the most common presenting symptom of supratentorial cerebral cavernous malformations (CCMs) and progress to medically refractory epilepsy in 40% of patients. Predictors of seizure freedom in the resection of CCMs are incompletely understood.
The authors systematically reviewed the published literature on seizure freedom following the resection of supratentorial CCMs in patients presenting with seizures. Seizure outcomes were stratified across 12 potential prognostic variables. A total of 1226 patients with supratentorial CCMs causing seizures were identified across 31 predominantly retrospective studies; 361 patients had medically refractory epilepsy.
Seventy-five percent of the patients were seizure free after microsurgical lesion removal, whereas 25% continued to have seizures. All patients had had preoperative seizures and > 6 months of postoperative follow-up. Modifiable predictors of postoperative seizure freedom included gross-total resection (OR 36.6, 95% CI 8.5–157.5) and surgery within 1 year of symptom onset (OR 1.83, 95% CI 1.30–2.58). Additional prognostic indicators of a favorable outcome were a CCM size < 1.5 cm (OR 15.4, 95% CI 5.2–45.4), the absence of multiple CCMs (OR 2.02, 95% CI 1.13–3.60), medically controlled seizures (OR 2.38, 95% CI 1.29–4.39), and the lack of secondarily generalized seizures (OR 3.33, 95% CI 2.09–5.30). Other factors, including extended resection of the hemosiderin ring, were not significantly predictive.
In the surgical treatment of supratentorial CCMs, gross-total resection and early operative intervention may improve seizure outcome. While surgery should not be considered the first-line treatment for CCM-related epilepsy, it is important to understand the variables associated with seizure freedom in CCM resection given the considerable morbidity and diminished quality of life associated with epilepsy.