A Novel Mesial Temporal Stereotactic Coordinate System

TECHNICAL NOTE J Neurosurg 130:67–75, 2019

A novel mesial temporal stereotactic coordinate system

Kai J. Miller, MD, PhD,1 Casey H. Halpern, MD,1 Mark F. Sedrak, MD,1,2 John A. Duncan III, MD, PhD,2 and Gerald A. Grant, MD1

1Department of Neurosurgery, Stanford University, Stanford; and 2Department of Neurosurgery, Kaiser Permanente, Redwood City, California

OBJECTIVE Stereotactic laser ablation and neurostimulator placement represent an evolution in staged surgical intervention for epilepsy. As this practice evolves, optimal targeting will require standardized outcome measures that compare electrode lead or laser source with postprocedural changes in seizure frequency. The authors propose and present a novel stereotactic coordinate system based on mesial temporal anatomical landmarks to facilitate the planning and delineation of outcomes based on extent of ablation or region of stimulation within mesial temporal structures. METHODS The body of the hippocampus contains a natural axis, approximated by the interface of cornu ammonis area 4 and the dentate gyrus. The uncal recess of the lateral ventricle acts as a landmark to characterize the anterior- posterior extent of this axis. Several volumetric rotations are quantified for alignment with the mesial temporal coordinate system. First, the brain volume is rotated to align with standard anterior commissure–posterior commissure (AC-PC) space. Then, it is rotated through the axial and sagittal angles that the hippocampal axis makes with the AC-PC line. RESULTS Using this coordinate system, customized MATLAB software was developed to allow for intuitive standard- ization of targeting and interpretation. The angle between the AC-PC line and the hippocampal axis was found to be approximately 20°–30° when viewed sagittally and approximately 5°–10° when viewed axially. Implanted electrodes can then be identified from CT in this space, and laser tip position and burn geometry can be calculated based on the intra- operative and postoperative MRI. CONCLUSIONS With the advent of stereotactic surgery for mesial temporal targets, a mesial temporal stereotactic system is introduced that may facilitate operative planning, improve surgical outcomes, and standardize outcome assessment. https://thejns.org/doi/abs/10.3171/2017.7.JNS162267 KEY WORDS stereotaxy; hippocampus; amygdala; epilepsy; stereotactic laser ablation; responsive neurostimulation; surgical technique

pilepsy is a disease of abnormal electrical signal However, temporal lobectomy and selective amygda- initiation and propagation throughout the brain, lohippocampectomy for resective therapy are not without affecting nearly 1% of the American population.7 side effects, and are associated with naming difficulty, EAbout 33% of epileptic patients are resistant to medica- decrease in verbal memory, and (rarely) amnesia.19 In this tion (having failed 2 or more appropriately dosed antiepi- context, 2 new stereotactic interventions have emerged in leptic drugs), requiring surgical intervention in an attempt an effort to preserve cognitive function, while still preserv- to control seizure frequency and severity.9,17,18,21 Temporal ing seizure freedom or reduction: MR-guided laser ther- lobe epilepsy is the most common form of localized (focal moablation, and electrical stimulation (Fig. 1). Stereotactic or partial) epilepsy,16 and surgical intervention provides laser ablation of the amygdalohippocampal complex and superior outcomes compared with prolonged medical ther- adjacent structures (stereotactic laser amygdalohippocam- apy.12,31 potomy [SLAH]) is performed by cannulated placement

ABBREVIATIONS AC-PC = anterior commissure–posterior commissure; CA4 = cornu ammonis area 4; RNS = responsive neurostimulator; SLAH = stereotactic laser amygdalohippocampotomy. SUBMITTED August 29, 2016. ACCEPTED July 6, 2017. INCLUDE WHEN CITING Published online January 26, 2018; DOI: 10.3171/2017.7.JNS162267.

©AANS 2019, except where prohibited by US copyright law J Neurosurg Volume 130 • January 2019 67

Unauthenticated | Downloaded 10/09/21 12:16 PM UTC K. J. Miller et al. of a fiber-optic filament within a target brain region. The for laser ablation with minimal neuropsychiatric side ef- region is then heated under direct visualization, using real- fects. If clear indications can be found, then this coordi- time MR thermography, stopping when the desired volume nate system could be used as a guide for surgical planning of brain has been heated beyond a set threshold.32 SLAH in much the same way as the anterior commissure–pos- has been found to provide seizure control that approaches terior commissure (AC-PC) system is currently used for that of open temporal lobectomy or selective amygdalohip- structures surrounding the third ventricle.27 pocampectomy, while sparing object recognition and naming function.10 Patients with epileptic foci localized to the Methods mesial temporal lobe are sometimes excluded from SLAH or resection in the case of bilateral disease, or if they have The following is a description of the procedure for ob- verbal decline or global memory deficit during selective taining coordinates in the mesial temporal stereotactic co- amytal injection (the Wada test).1,23 For these patients, re- ordinate system in a series of steps. sponsive or tonic electrical stimulation of the seizure focus via stereotactically placed depth electrodes can provide a Identify AC-PC Coordinate Space reduction in seizure frequency and severity.4,6,20,28,29 We begin by determining the landmarks necessary to Stereotactic targeting for these approaches is evolving, transform to AC-PC space. The AC-PC line is identified in although it is currently prescribed for general anatomical the standard fashion.27 First, the AC and PC are identified structures rather than a landmark-based coordinate sys- on the MR image. Then several midline points are identi- tem. The present standard for directly targeting the amyg- fied. A rotation matrix is calculated to align the structural dalohippocampal complex for SLAH is defined by pass- MRI with AC-PC coordinate space. ing the filament through the long axis of the hippocampal body, traversing the pes hippocampi, and extending into Identify Hippocampal Landmarks the amygdala anteriorly; the goal for the treatment region using this standard is a tubular thermal lesion, extending We then identify hippocampal structures. The body of (in cylindrical form) along a single axis from the amyg- the hippocampus provides a natural, intuitive axis that can dala extending posteriorly through the hippocampus to the be identified on different imaging modalities (Fig. 2). This transverse level of the lateral mesencephalic sulcus.32 Re- is approximated by the superolateral margin of the inter- sults have been quantified as percentage of amygdalohip- face of the cornu ammonis area 4 (CA4) and the dentate pocampal complex treated (e.g., 60%), rather than the lo- gyrus, from the interpeduncular cistern to the superior col- 11,15,30 cation treated. For stimulation of the hippocampus, there liculus. This is easily identified on coronal sections. are no established standards. Angles between the AC-PC line and the hippocampal axis We believe that outcomes of these procedures may from axial (q) and sagittal (j) views are then calculated improve by adoption of a stereotactic coordinate system explicitly (Fig. 3). The uncal recess of the lateral ventricle that is based on landmarks of the mesial temporal lobe. In (Fig. 4) is an ideal anterior-posterior landmark:11,22,32 it is this paper we propose one such system, and have created robust (easily visible on both T1- and T2-weighted axial an open-source, freely available software package to test MRI), and its position is relatively conserved with both it. We believe that there is a need for anatomically based atrophy and hydrocephalus.5 It marks the division between retrospective analysis in a coordinate-based system such the anterior extent of the hippocampal head and the poste- as this one, particularly for cases of “nonlesional” mesial rior aspect of the overlying amygdala. The measurements temporal epilepsy (e.g., no sclerosis, dysplasia). This will illustrated in Figs. 2–4 were performed on 18 patients be relevant for a more complete understanding of proper with epilepsy (range 23–61 years old; 10 women) whose loci for stimulation, as well as which regions are optimal clinical data had been approved for use by the IRBs of

FIG. 1. A: Stereotactic approaches to the hippocampus, amygdala, and adjacent structures have emerged as a revolution in the surgical treatment of mesial temporal lobe sclerosis. B: Stereotactically placed fiber-optic probes are used for laser ablation of the hippocampus and adjacent structures under MRI guidance (Visualase/Medtronic or Monteris). C: Recording/stimulating electrodes are placed stereotactically for responsive neurostimulation (Neuropace). Figure is available in color online only.

68 J Neurosurg Volume 130 • January 2019

Unauthenticated | Downloaded 10/09/21 12:16 PM UTC K. J. Miller et al.

FIG. 2. Hippocampal axis. The body of the hippocampus contains a natural, intuitive axis. This is approximated by the interface of CA4 and the dentate gyrus, from the interpeduncular cistern to the superior colliculus. A: The region of the hippocampus lies within the green oval. The hippocampal axis is noted by a green dot. Modified from Gray’s Anatomy.15 B: This histological prepara- tion of the hippocampus illustrates the target for the hippocampal axis (green circle) at the lateral CA4 subfield where it interfaces with the dentate gyrus. Modified from Mueller SG, Weiner MW: Selective effect of age, Apo e4, and Alzheimer’s disease on hippocampal subfields.Hippocampus 19:558–564, 2009. Published with permission from John Wiley & Sons. C: Approximate cross sections of D–F. D–F: Pseudocoronal cross sections showing the target of the hippocampal axis with green circles on T1- (upper) and T2-weighted (lower) MRI. Figure is available in color online only. the University of Washington (12 random, anonymized Kaiser Permanente (6 patients who underwent bilateral re- patients with epilepsy whose imaging is easily accessible sponsive neurostimulator [RNS] placement). Patients gave and available [https://purl.stanford.edu/zk881ps0522]) and appropriate consent according to IRB directives.

FIG. 3. Angles defined by the hippocampal axis. A: The angle between the AC-PC line and the hippocampal axis when viewed sagittally (j) is typically approximately 20°–30° (mean 25° ± 6°), as shown by an angular histogram of 18 epileptic patients with left and right hippocampi combined. B: The angle between a parasagittal line (parallel to the AC-PC) and the hippocampal axis when viewed axially (q) is approximately 5°–10° (mean 3° ± 9°, significantly different from 0°, p = 0.003 by resampling), as shown by the angular histogram of 12 epileptic patients with left and right hippocampi combined (after reflection of left hippocampi to right). There was no difference in j (p = 0.587) or q (p = 0.652) between left and right hippocampi (after reflecting sign of q for left hippocampi).

J Neurosurg Volume 130 • January 2019 69

Unauthenticated | Downloaded 10/09/21 12:16 PM UTC K. J. Miller et al.

FIG. 4. The uncal recess as a landmark to characterize anterior-posterior extent of this axis. A: Parasagittal and axial sections through the uncal recess are shown, with relationship to the lateral ventricle, hippocampus, and amygdala. B and C: The sagittal (B) and axial (C) relationships are shown in greater detail. D and E: Appearance of the uncal recess (red circle) on T1- (D) and T2-weighted (E) MRI. A–C modified from Duvernoy HM: The Human Hippocampus: Functional Anatomy, Vascularization and Se- rial Sections with MRI. Berlin: Springer, 2005. With permission from Springer.

Perform Transformation to Hippocampal Stereotaxic lyze-image). All other images are then coregistered and Space resliced into this image using normalized mutual infor- There are several volumetric rotations necessary for mation (Fig. 6).13 Pre- and postprocedural images are alignment with the mesial temporal coordinate system visualized simultaneously, and electrode positions, fiber- (Fig. 5). First, the rotations necessary to align the native optic trajectories, or burn regions are selected and export- MRI with the standard AC-PC space are calculated. Next, ed into data files so that they can later be used for averag- the rotations required to rotate the AC-PC line into the ing across patients. A customized graphical user interface hippocampal axis are calculated, first by rotating from an package (the “Hippotaxy” MATLAB-based code) allows axial perspective through the angle q, and then by rotating for the automation of this process, and is available along through the angle j' from a pseudosagittal view. Note that with an instructional guide and video illustrations (http:// this view will deviate slightly from a true sagittal view, purl.stanford.edu/pn316qg0195). The freely available and j' is a corrected angle from j, because of the pre- MATLAB-based SPM12 software is used for DICOM ceding axial (q) rotation. Note that only 1 equivalent rota- to NIfTI conversion and coregistration/reslicing (http:// tion and reslicing of the MRI volume need be performed, www.fil.ion.ucl.ac.uk/spm/software/).2,13 whose rotation matrix is the multiplicative product of the individual rotation matrices. Following rotation, the vol- Illustration of Mesial Temporal Stereotaxy in a Small ume is translated to have the coordinate system origin Cohort along the hippocampal axis, with anterior-posterior origin To provide a small practical demonstration of how at the uncal recess. mesial temporal stereotaxy can be useful, we quantified electrode placement in 6 patients who underwent bilateral Practical Implementation With Customized Software 4-contact RNS lead placements for epilepsy. The Kaiser All pre- and postprocedural MR and CT imaging is Permanente IRB approved all patient data for retrospective converted from standard DICOM (.dcm) directory to analysis, and consent was obtained from patients accord- NIfTI (.nii) format. Then, the anterior/posterior commis- ingly. For these 12 leads, electrode positions in AC-PC and sures, several distant midline points, several hippocam- mesial temporal stereotactic space were measured with pal axis points, and the uncal recess are selected manu- the Hippotaxy software. Comparisons of electrode spatial ally from a preoperative anatomical T1- or T2-weighted spread were made by performing a principal component image. This image is then resliced into 1 mm3 mesial decomposition to determine the principal axes of the distri- temporal (or AC-PC, if desired) stereotactic space using butions. The eigenvalue associated with each of these prin- an affine transformation (https://www.mathworks.com/ cipal axes is used as the measure of spatial spread along matlabcentral/fileexchange/8797-tools-for-nifti-and-ana- the associated axis (Fig. 7). For each permutation in the

70 J Neurosurg Volume 130 • January 2019

Unauthenticated | Downloaded 10/09/21 12:16 PM UTC K. J. Miller et al.

FIG. 5. Transformation to the mesial temporal stereotactic coordinate system. A: An illustration of the volumetric rotations necessary for alignment with the mesial temporal coordinate system. First, the brain is rotated to align with standard AC-PC space. Next, the volumetric matrix is rotated about the z-axis from AC-PC space into the hippocampal axis (green line), which can be viewed axially as the angle q. Finally, the volume is rotated through the angle between the AC-PC line and the hippocampal axis when viewed sagittally (j). Note that, in practice—and in the software package—only 1 equivalent rotation and reslicing of the volume need be performed, whose rotation matrix is the multiplicative product of the individual rotation matrices. B: View of the isolated hippocampus volumetrically, with the hippocampal (anterior-posterior) axis shown in green and the medial-lateral axis shown in orange. They intersect at the origin, where the superior-inferior coordinate equals zero. C: The plane at the level where the superior-inferior coordinate equals zero in the mesial temporal stereotactic coordinate system, with the other axes colored as in panel B. Figure is available in color online only. resampling analysis illustrated in Fig. 7E, the same random is useful, we characterized a small cohort of 6 consecutive subset of two-thirds of electrodes was picked in the AC-PC bilateral RNS placements for bitemporal epilepsy. Because and mesial temporal stereotactic coordinate system, and the placements were all performed by the same experienced the principal component decomposition (with associated surgeons (J.A.D. and M.F.S. jointly) for the same indica- eigenvalues) was performed on the subset. One thousand tion, the planning and surgical procedure is as optimally resampling permutations were performed. reproducible as we might be able to expect, based on direct targeting via visual inspection of the MRI. Therefore, we Results can use this for a simple comparison of our proposed mesial temporal stereotactic space versus the AC-PC stereo- Using the customized software we call Hippotaxy, the tactic space, which is the current standard for stereotactic midline point and the anterior/posterior commissures targeting and assessment. As shown in Fig. 7, the spread in were easily identified on the axial and coronal MR images distribution is significantly more compact for the case of (Fig. 2). Similarly, the body of the hippocampus was easily mesial temporal stereotaxy (p < 0.001, p < 0.001, and p = identified, even in the case of mesial temporal sclerosis, on 0.021 for principal dimensions 1–3, respectively). In Fig. 8, both the right and left sides. As noted in Fig. 3, the aver- we show simple histograms of the electrode placements in age angle between the AC-PC line and the hippocampal mesial temporal stereotactic space. axis when viewed sagittally (j) was 25° ± 6° (18 patients, left and right hippocampi combined). The angle between a parasagittal line (parallel to the AC-PC) and the hippo- Discussion campal axis when viewed axially (q) was 3° ± 9° laterally Early surgical intervention for mesial temporal lobe rotated (18 patients, with left hippocampi reflected to the epilepsy benefits disease progression over medical therapy right, significantly different from ° 0 ; p = 0.003 by per- alone,12,31 and these stereotactic procedures minimize the mutation resampling). There was no difference in j (p = negative sequelae.4,10 Laser ablation of the mesial temporal 0.587) or q (p = 0.652) between left and right hippocampi lobe has demonstrated efficacy in both adult and pediatric (after reflecting left hippocampi to the right). As shown in patients.8,32 Laser ablation and stimulation are each now Fig. 4, the uncal recess was easily identifiable. The trans- used as either primary therapies or adjuvant therapies fol- formation to mesial temporal stereotactic space was ro- lowing surgery for lateralized temporal onset of seizures bust and reliably reveals the long axis of the hippocampus in patients with medically refractory epilepsy. In the case (Figs. 5 and 6). Anatomical points and volumes are identi- of bitemporal epilepsy, one could ablate the nondominant fied and exported to MATLAB data files and raw text files mesial temporal lobe and place an RNS on the dominant for later averaging. side. To illustrate why this mesial temporal stereotactic space Occipital approaches to the hippocampus and adja-

J Neurosurg Volume 130 • January 2019 71

Unauthenticated | Downloaded 10/09/21 12:16 PM UTC K. J. Miller et al.

FIG. 6. The Hippotaxy software is a pair of custom programs that are freely available MATLAB-based graphical user interfaces (GUIs). A: Illustration of parsing a T1-weighted MR image, selected along the hippocampal axis. This GUI is used for browsing MR and CT images, selecting mesial temporal landmarks, coregistering images, and obtaining resliced images in both AC-PC and mesial temporal stereotactic space. B: A second GUI is used for simultaneous viewing of coregistered images (pre-/postprocedural on the left/right, respectively). It can be used for selecting electrode locations and burn regions viewed in this mesial temporal stereotactic space (or AC-PC if desired). Selected locations and regions can be exported to a text file or MATLAB data file, where their values in this mesial temporal stereotactic space can be aggregated across many patients. Figure is available in color online only.

72 J Neurosurg Volume 130 • January 2019

Unauthenticated | Downloaded 10/09/21 12:16 PM UTC K. J. Miller et al.

FIG. 7. A comparison of AC-PC space and mesial temporal stereotactic space in a small cohort. Six consecutive bilateral posterior- approach RNS leads were implanted (12 four-electrode leads, 48 total electrodes), and here we ask: Is there a way of representing this surgeon’s electrode placement that captures his direct targeting strategy? A and B: Two examples of electrode placement are shown alongside the outlined hippocampus. C: The overlaid electrodes/hippocampi from A and B are shown. The spread in data along the principal dimensions (Dim) of the combined distributions of electrodes is indicated beneath. D: Similar to panel C, but after the electrodes have been transformed to mesial temporal stereotactic space, showing how the data spread changes. The spread in data along all 3 principal dimensions (in descending order) was smaller in the mesial temporal stereotactic space than in the AC-PC space. E: Permutation testing was performed by randomly selecting two-thirds of the data (32 electrodes) and recal- culating principal dimensions and spread along each dimension 1000 times, showing that electrode positions significantly favor the mesial temporal stereotactic space (p values of < 0.001, < 0.001, and 0.021 for dimensions 1–3, respectively). Because the surgeon was directly targeting mesial temporal structures along the length of the hippocampus, use of mesial temporal stereotactic space clusters the full complement of electrodes more tightly than does use of AC-PC space. Figure is available in color online only. cent structures evolved from depth electrode approaches tion to optimal ablation or electrode placement loci. We for electrophysiological recording in seizure monitoring. are as yet not sure what the best regional structures within These approaches, pioneered by the Spencers,24–26 gener- the mesial temporal lobe will be, and our hope is that op- ally correspond to our “principal axis” to maximize the timal trajectories will emerge from a probabilistic map number of recording leads in the hippocampus. This axis after anatomical analysis of a large cohort is compared is also commonly referred to as the “long axis of the hip- with seizure semiology and postoperative outcome. It may pocampus.”32 The “hippocampal axial plane” described by be that these optimal trajectories correspond to transverse Beaurain and colleagues3 shares some similarity to our co- (transtemporal) or oblique approaches. This system will ordinate system, but is parasagittal, and therefore oblique allow comparison of targeting volume with seizure reduc- to the long axis of the hippocampus. It should be noted tion and postoperative deficit. If useful, this coordinate that recent series with laser ablation do not aim along the system and these trajectories could be easily adapted and principal axis, but rather favor a steeper, lateral-to-medial integrated into existing commercial stereotactic guidance approach.32 This allows for more extensive ablation of the platforms, as well as robotic targeting systems.14 uncus, at the expense of posterior portions of the hippo- The hippocampus has widespread and diverse corti- campal body. cal projections. It may be that slightly different semiology The choice of coordinate system is not meant to align implies that a different mesial temporal structure is gen- with the optimal trajectory, but to be robust with respect to erating or propagating the seizure. This mesial temporal hippocampal anatomy across patients. Of important note, coordinate system approach could be used to develop an the axes of this coordinate system, particularly the long/ electrophysiological map of the hippocampus. With careful principal axis of the hippocampus, need not have any rela- analysis, we might actually begin to be able to understand

J Neurosurg Volume 130 • January 2019 73

Unauthenticated | Downloaded 10/09/21 12:16 PM UTC K. J. Miller et al.

FIG. 8. A simple illustration of the utility of the mesial temporal stereotactic space: quantitatively describing placement charac- teristics of a single surgical practice. The distribution of 48 placed RNS electrodes (i.e., the 12 leads from Fig. 7) is shown in mesial temporal stereotactic space (MR image is from a representative patient). A: A pseudoaxial slice through the origin of the coordinate system is shown (origin marked by red dot). Examination of the histogram of positions along the principal axis of the hippocampus (blue bars) shows that 6 electrodes were placed anterior to the hippocampus (e.g., the anterior-most electrode in half of the leads extended past the uncal recess). As seen in the green (medial-lateral) histogram, electrodes tended to be in the lateral aspect of, or lateral to, the hippocampus. B: In the orange histogram, we can see that electrode positions tend to be slightly below the long axis of the hippocampus, and not extend above, as might be expected given the location of the temporal horn of the lateral ventricle. Figure is available in color online only. clustered “morphologies”—combined semiological and epilepsy (e.g., no sclerosis, dysplasia), there may be differ- anatomical findings—that implicate specific subregions ent focal targets for stimulation or lesioning, depending on of the amygdalohippocampal complex. These subregions the semiology. might act as primary generators of seizures, a conduit for Stereotactic placement of stimulating electrodes and focus elsewhere, or a kindled secondary focus. laser filaments has emerged as an important component In collaboration with colleagues at other institutions, of epilepsy therapy. Optimal stereotactic targeting will re- we are currently validating this hippocampal stereotaxic quire standardized outcome measures that compare elec- space in a cohort of patients in a retrospective fashion to trode lead or laser source with postprocedural changes in better characterize the extent of laser ablation as well as seizure frequency. However, there is no standardized ap- placement of depth electrodes for neurostimulation. We proach for how this should be performed for the hippo- anticipate that this will be the first step, but that hippocampus and surrounding structures. We therefore describe campal stereotactic approaches will evolve as stereotac- a referential stereotactic coordinate system based on me- tic surgery for epilepsy becomes more widely adopted. In sial temporal anatomical landmarks, taking advantage of addition to evaluation of efficacy and cognitive sequelae a natural axis through the body of the hippocampus and a following stereotaxic surgery, there should also be com- reliable anchor point provided by the uncal recess of the parison with preoperative anatomic variation and seizure lateral ventricle. This coordinate system may facilitate semiology. Standardized targeting in this coordinate sys- operative planning, improve surgical outcomes, and stan- tem may be developed for more precise intervention, and dardize outcome assessment. also to link anatomy to specific seizure semiology (rather than just general localization to the mesial temporal lobe). There may in fact be different hippocampal or amygda- Acknowledgments lar targets based on the seizure semiology or electroen- We are grateful to our patients, to the epilepsy neurology team, cephalography, or for variations in sclerosis, which are and for the mentorship of Lawrence Shuer, who has provided con- only revealed by systematic analysis of many patients in a stant support and advice to ensure safe and effective adoption of common space. In the case of nonlesional mesial temporal these novel surgical approaches for epilepsy. Prior to publication,

74 J Neurosurg Volume 130 • January 2019

Unauthenticated | Downloaded 10/09/21 12:16 PM UTC K. J. Miller et al. the software package was evaluated by Allen Ho, Dario Englot, and sensus proposal by the ad hoc Task Force of the ILAE Com- Adam Hebb, who also provided helpful conversation regarding the mission on Therapeutic Strategies. Epilepsia 51:1069–1077, manuscript and larger context of this project. We appreciate conver- 2010 (Erratum in Epilepsia 51:1922, 2010) sations with Melanie Hayden, Kelly Foote, and Jeffrey Ojemann. 19. Meador KJ: Cognitive outcomes and predictive factors in epilepsy. Neurology 58 (8 Suppl 5):S21–S26, 2002 References 20. Miller KJ, Burns TC, Grant GA, Halpern CH: Responsive stimulation of motor cortex for medically and surgically re- 1. Abosch A, Bernasconi N, Boling W, Jones-Gotman M, Pou- fractive epilepsy. Seizure 33:38–40, 2015 lin N, Dubeau F, et al: Factors predictive of suboptimal sei- 21. Moshé SL, Perucca E, Ryvlin P, Tomson T: Epilepsy: new zure control following selective amygdalohippocampectomy. advances. Lancet 385:884–898, 2015 J Neurosurg 97:1142–1151, 2002 22. Mueller SG, Weiner MW: Selective effect of age, Apo e4, and 2. Ashburner J, Friston KJ: Unified segmentation. Neuroimage Alzheimer’s disease on hippocampal subfields. Hippocam- 26:839–851, 2005 pus 19:558–564, 2009 3. Beaurain J, Dormont D, Semah F, Hasboun D, Baulac M: 23. Spencer D, Burchiel K: Selective amygdalohippocampec- Hippocampal formations imaging with axial sections parallel tomy. Epilepsy Res Treat 2012:382095, 2012 to their longitudinal axis. Magn Reson Imaging 12:139–148, 24. Spencer SS: Depth electroencephalography in selection of 1994 refractory epilepsy for surgery. Ann Neurol 9:207–214, 1981 4. Bergey GK, Morrell MJ, Mizrahi EM, Goldman A, King-Ste- 25. Spencer SS, Spencer DD, Williamson PD, Mattson R: Com- phens D, Nair D, et al: Long-term treatment with responsive bined depth and subdural electrode investigation in uncon- brain stimulation in adults with refractory partial seizures. trolled epilepsy. Neurology 40:74–79, 1990 Neurology 84:810–817, 2015 26. Spencer SS, Spencer DD, Williamson PD, Mattson RH: 5. Bigler ED, Blatter DD, Anderson CV, Johnson SC, Gale SD, The localizing value of depth electroencephalography in 32 Hopkins RO, et al: Hippocampal volume in normal aging and patients with refractory epilepsy. Ann Neurol 12:248–253, traumatic brain injury. AJNR Am J Neuroradiol 18:11–23, 1982 1997 27. Starr PA, Vitek JL, DeLong M, Bakay RA: Magnetic reso- 6. Boon P, Vonck K, De Herdt V, Van Dycke A, Goethals M, nance imaging-based stereotactic localization of the globus Goossens L, et al: Deep brain stimulation in patients with pallidus and subthalamic nucleus. Neurosurgery 44:303– refractory temporal lobe epilepsy. Epilepsia 48:1551–1560, 314, 1999 2007 28. Sun FT, Morrell MJ, Wharen RE Jr: Responsive cortical 7. Centers for Disease Control and Prevention (CDC): Epilepsy stimulation for the treatment of epilepsy. Neurotherapeutics in adults and access to care—United States, 2010. MMWR 5:68–74, 2008 Morb Mortal Wkly Rep 61:909–913, 2012 29. Velasco AL, Velasco F, Velasco M, María Núñez J, Trejo D, 8. Curry DJ, Gowda A, McNichols RJ, Wilfong AA: MR-guid- García I: Neuromodulation of epileptic foci in patients with ed stereotactic laser ablation of epileptogenic foci in children. non-lesional refractory motor epilepsy. Int J Neural Syst Epilepsy Behav 24:408–414, 2012 19:139–147, 2009 9. Del Felice A, Beghi E, Boero G, La Neve A, Bogliun G, De 30. Wen HT, Rhoton AL Jr, de Oliveira E, Cardoso AC, Tedeschi Palo A, et al: Early versus late remission in a cohort of pa- H, Baccanelli M, et al: Microsurgical anatomy of the tempo- tients with newly diagnosed epilepsy. Epilepsia 51:37–42, ral lobe: part 1: mesial temporal lobe anatomy and its vascu- 2010 lar relationships as applied to amygdalohippocampectomy. 10. Drane DL, Loring DW, Voets NL, Price M, Ojemann JG, Neurosurgery 45:549–592, 1999 Willie JT, et al: Better object recognition and naming 31. Wiebe S, Blume WT, Girvin JP, Eliasziw M: A randomized, outcome with MRI-guided stereotactic laser amygdalohip- controlled trial of surgery for temporal-lobe epilepsy. N Engl pocampotomy for temporal lobe epilepsy. Epilepsia 56:101– J Med 345:311–318, 2001 113, 2015 32. Willie JT, Laxpati NG, Drane DL, Gowda A, Appin C, Hao 11. Duvernoy HM: The Human Hippocampus: Functional C, et al: Real-time magnetic resonance-guided stereotactic Anatomy, Vascularization and Serial Sections with MRI. laser amygdalohippocampotomy for mesial temporal lobe Berlin: Springer, 2005 epilepsy. Neurosurgery 74:569–585, 2014 12. Engel J Jr, McDermott MP, Wiebe S, Langfitt JT, Stern JM, Dewar S, et al: Early surgical therapy for drug-resistant temporal lobe epilepsy: a randomized trial. JAMA 307:922–930, 2012 13. Friston KJ, Holmes AP, Worsley KJ, Poline J, Frith CD, Frackowiak RS: Statistical parametric maps in functional Disclosures imaging: a general linear approach. Hum Brain Mapp The authors report no conflict of interest concerning the materi- 2:189–210, 1994 als or methods used in this study or the findings specified in this 14. Gonzalez-Martinez J, Vadera S, Mullin J, Enatsu R, Alexo- paper. poulos AV, Patwardhan R, et al: Robot-assisted stereotactic laser ablation in medically intractable epilepsy: operative Author Contributions technique. Neurosurgery 10 (Suppl 2):167–173, 2014 15. Gray H: Anatomy, Descriptive and Surgical. Philadelphia: Conception and design: Miller. Acquisition of data: all authors. Lea Brothers & Co, 1893 Analysis and interpretation of data: Miller. Drafting the article: 16. Holmes G, Sirven J, Fisher RS: Temporal lobe epilepsy. Miller. Critically revising the article: all authors. Reviewed sub- Epilepsy.com. (http://www.epilepsy.com/learn/types- mitted version of manuscript: all authors. Approved the final ver- epilepsy-syndromes/temporal-lobe-epilepsy-aka-tle) [Ac- sion of the manuscript on behalf of all authors: Miller. Statistical cessed September 25, 2017] analysis: Miller. 17. Jobst BC, Cascino GD: Resective epilepsy surgery for drug- resistant focal epilepsy: a review. JAMA 313:285–293, 2015 Correspondence 18. Kwan P, Arzimanoglou A, Berg AT, Brodie MJ, Hauser WA, Kai J. Miller: Stanford University, Stanford, CA. kai.miller@ Mathern G, et al: Definition of drug resistant epilepsy: con- stanford.edu.

J Neurosurg Volume 130 • January 2019 75

Unauthenticated | Downloaded 10/09/21 12:16 PM UTC