Medically resistant pediatric insular-opercular/perisylvian epilepsy. Part 1: invasive monitoring using the parasagittal transinsular apex depth electrode

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OBJECTIVE

Insular lobe epilepsy (ILE) is an under-recognized cause of extratemporal epilepsy and explains some epilepsy surgery failures in children with drug-resistant epilepsy. The diagnosis of ILE usually requires invasive investigation with insular sampling; however, the location of the insula below the opercula and the dense middle cerebral artery vasculature renders its sampling challenging. Several techniques have been described, ranging from open direct placement of orthogonal subpial depth and strip electrodes through a craniotomy to frame-based stereotactic placement of orthogonal or oblique electrodes using stereo-electroencephalography principles. The authors describe an alternative method for sampling the insula, which involves placing insular depth electrodes along the long axis of the insula through the insular apex following dissection of the sylvian fissure in conjunction with subdural electrodes over the lateral hemispheric/opercular region. The authors report the feasibility, advantages, disadvantages, and role of this approach in investigating pediatric insular-opercular refractory epilepsy.

METHODS

The authors performed a retrospective analysis of all children (< 18 years old) who underwent invasive intracranial studies involving the insula between 2002 and 2015.

RESULTS

Eleven patients were included in the study (5 boys). The mean age at surgery was 7.6 years (range 0.5–16 years). All patients had drug-resistant epilepsy as defined by the International League Against Epilepsy and underwent comprehensive noninvasive epilepsy surgery workup. Intracranial monitoring was performed in all patients using 1 parasagittal insular electrode (1 patient had 2 electrodes) in addition to subdural grids and strips tailored to the suspected epileptogenic zone. In 10 patients, extraoperative monitoring was used; in 1 patient, intraoperative electrocorticography was used alone without extraoperative monitoring. The mean number of insular contacts was 6.8 (range 4–8), and the mean number of fronto-parieto-temporal hemispheric contacts was 61.7 (range 40–92). There were no complications related to placement of these depth electrodes. All 11 patients underwent subsequent resective surgery involving the insula.

CONCLUSIONS

Parasagittal transinsular apex depth electrode placement is a feasible alternative to orthogonally placed open or oblique-placed stereotactic methodologies. This method is safe and best suited for suspected unilateral cases with a possible extensive insular-opercular epileptogenic zone.

ABBREVIATIONSECoG = electrocorticography; EEG = electroencephalography; FLE = frontal lobe epilepsy; ILE = insular lobe epilepsy; IOZ = ictal onset zone; MCA = middle cerebral artery; OTO = orthogonal transopercular; PLE = parietal lobe epilepsy; TFO = transfrontal oblique; TLE = temporal lobe epilepsy; TPO = transparietal oblique.

Abstract

OBJECTIVE

Insular lobe epilepsy (ILE) is an under-recognized cause of extratemporal epilepsy and explains some epilepsy surgery failures in children with drug-resistant epilepsy. The diagnosis of ILE usually requires invasive investigation with insular sampling; however, the location of the insula below the opercula and the dense middle cerebral artery vasculature renders its sampling challenging. Several techniques have been described, ranging from open direct placement of orthogonal subpial depth and strip electrodes through a craniotomy to frame-based stereotactic placement of orthogonal or oblique electrodes using stereo-electroencephalography principles. The authors describe an alternative method for sampling the insula, which involves placing insular depth electrodes along the long axis of the insula through the insular apex following dissection of the sylvian fissure in conjunction with subdural electrodes over the lateral hemispheric/opercular region. The authors report the feasibility, advantages, disadvantages, and role of this approach in investigating pediatric insular-opercular refractory epilepsy.

METHODS

The authors performed a retrospective analysis of all children (< 18 years old) who underwent invasive intracranial studies involving the insula between 2002 and 2015.

RESULTS

Eleven patients were included in the study (5 boys). The mean age at surgery was 7.6 years (range 0.5–16 years). All patients had drug-resistant epilepsy as defined by the International League Against Epilepsy and underwent comprehensive noninvasive epilepsy surgery workup. Intracranial monitoring was performed in all patients using 1 parasagittal insular electrode (1 patient had 2 electrodes) in addition to subdural grids and strips tailored to the suspected epileptogenic zone. In 10 patients, extraoperative monitoring was used; in 1 patient, intraoperative electrocorticography was used alone without extraoperative monitoring. The mean number of insular contacts was 6.8 (range 4–8), and the mean number of fronto-parieto-temporal hemispheric contacts was 61.7 (range 40–92). There were no complications related to placement of these depth electrodes. All 11 patients underwent subsequent resective surgery involving the insula.

CONCLUSIONS

Parasagittal transinsular apex depth electrode placement is a feasible alternative to orthogonally placed open or oblique-placed stereotactic methodologies. This method is safe and best suited for suspected unilateral cases with a possible extensive insular-opercular epileptogenic zone.

Recent evidence has suggested that failure to recognize seizures arising from the insular cortex could be responsible for some cases of surgical failure in patients with frontal, temporal, or parietal lobe epilepsy.2,9,15–17,20,23,29,30 Insular seizures may mimic or coexist with seizures due to temporal or perisylvian epilepsy.4,29 Although a standard presurgical investigation may aid in suggesting an insular ictal onset zone (IOZ), confirmation of insular cortex epilepsy31 usually requires invasive investigation with insular coverage.9,15,16,23,33 This is especially true in children, in whom invasive investigation has been recommended to confirm insular lobe epilepsy (ILE) in all cases.13

Recent studies have justified invasive sampling of the insula, as insulectomy has been shown to be both safe and effective in treating ILE when performed alone or in combination with perisylvian corticectomy.10,12,14,19,20,24,28,33,37 However, the vast majority of literature pertains to adults, with few reports documenting the safety and efficacy of insular investigation or resection in children.13

Several methods have been used to perform invasive insular sampling for investigating drug-resistant epilepsy, each with their own advantages, disadvantages, and risks.1,8,9,13,24,33 Insular depth electrode electroencephalography (EEG) approaches include either orthogonal or oblique frame-based stereotactic methods1,15,16,27 or open, direct transsylvian implantation of orthogonally placed depth electrodes in,33 or strip24 electrodes on, the insula following microsurgical opening of the sylvian fissure. Frame-based stereotactic techniques include the stereotactic orthogonal transopercular (OTO) Talairach method3,13–16 or stereotactic parasagittal techniques through the frontal lobe (transfrontal oblique [TFO]),1,8,9 parietal lobe (transparietal oblique [TPO]),1,27 and any combinations of these stereotactic methods (TFO-TPO, TFO-TPO-OTO).26

We describe an alternative method for sampling the insula, in which an insular depth electrode is placed parasagittally down the long axis of the insula through the insular apex/limen insula following dissection of the sylvian fissure in conjunction with tailored hemispheric/opercular coverage with subdural electrodes. We report the feasibility and advantages and disadvantages of this approach in children with insular-opercular refractory epilepsy.

Methods

We performed a retrospective chart review of all patients who, between May 2009 and April 2015, underwent invasive investigation of the insula and perisylvian regions for drug-resistant epilepsy using the parasagittal transinsular apex electrode in addition to perisylvian strips/grids at Miami Children's Hospital. Miami Children's Hospital is a tertiary-care national and international referral hospital for drug-resistant epilepsy in children. All operations in this series were performed by a single surgeon (S.B.). We included all consecutive patients undergoing invasive insular investigation using the parasagittal transinsular apex depth electrode. All patients underwent a comprehensive epilepsy surgical workup as described previously.11,18 Briefly, this workup includes taking a complete history and performing neurological examination, neuropsychological evaluation, scalp video-electroencephalography (EEG) monitoring, and 3-T MRI. Ancillary testing with SPECT, FDG-PET, and source localization was performed in all cases.

Patient Selection and Indications

Invasive investigation and extent of resective surgery were decided in each case after discussion in a multidisciplinary epilepsy conference. In accordance with prior studies, indications for insular sampling included insular/perisylvian lesion and noninvasive, discordant data; perisylvian lesion with atypical semiology suggestive of an insular IOZ (e.g., laryngeal constriction and/or sensory symptoms); and prior failed nonlesional resective surgery with presurgical data indicating an insular IOZ.13,15,16,23 Based on these criteria, the decision to proceed with insular sampling during invasive investigation was based on a very high degree of suspicion of insular involvement, including a combination of early insular semiology, lesion involving the insula as exhibited on MRI, and suspected insula involvement as exhibited on PET and/or SPECT.

Operative Technique

Surgical Anatomy of the Insular Lobe

Detailed working knowledge of the insular lobe and sylvian fissure is critical for carrying out this technique. The surgical anatomy of the insular lobe and perisylvian region has been described in detail elsewhere (Fig. 1).34 The insula is a pyramid-shaped structure located in the depth of the sylvian fissure, as it forms the medial wall of the deep (operculo-insular) compartment of the sylvian fissure. Insular surface anatomy is important for planning electrode placement. The insula harbors 5 gyri, including 3 short gyri and 2 long gyri. Important insular surface landmarks are the insular pole, limen insulae, and insular apex. The insular pole is the most anteroinferior edge of the insula, essentially the point of the pyramid, located at the convergence of the 3 short gyri, which radiate supero-posteriorly from the insular pole. The insular pole is superior and lateral to the limen insulae, the site of the middle cerebral artery (MCA) bifurcation. The insular apex is the highest and most prominent portion of the insula laterally on the insular convexity and is usually located on the middle short gyrus, above and posterior to the insular apex, and above the limen insulae and MCA bifurcation. It is thus a readily available site for electrode insertion.

FIG. 1.
FIG. 1.

Cadaveric brain with frontal, parietal, and temporal opercula removed demonstrating insular anatomy. Acc. = accessory; alg = anterior long gyrus; Ant. = anterior; Apex = insular apex; asg = anterior short gyrus; ins. = insular; Li = limen insulae; msg = middle short gyrus; plg = posterior long gyrus; psg = posterior short gyrus; Sup. = superior; Transv. = transverse.

Knowledge of the relationship of the insular topographical anatomy to the sylvian fissure is also important. Whereas the limen insulae is located deep to the temporal operculum, the superior anterior and middle short gyri are usually located below the pars opercularis. The pars triangularis covers mostly the upper anterior short gyrus. Thus, the posterior ramus of the superficial sylvian fissure, adjacent to the pars triangularis, will expose the anterior/middle short gyri and anteroinferior insula. The insular apex is essentially located directly below the sylvian fissure, between the temporal operculum and pars triangularis/opercularis. Figure 2 is a medical illustration demonstrating the different techniques for insular sampling.

FIG. 2.
FIG. 2.

Medical illustration demonstrating the different techniques for insular sampling. Copyright Sanjiv Bhatia. Published with permission. SEEG = stereo-EEG.

Patient Positioning and Craniotomy

With the patient supine, the head is rotated 45° to 60° to the contralateral side and fixed in place with a 3-point Mayfield head holder (Video 1 and Fig. 3B).

VIDEO 1. Video illustrating technique for placement of transsylvian parasagittal insular depth electrode for suspected ILE. alg = anterior long gyrus; asg = anterior short gyrus; FTP = fronto-temporo-parietal; ia = insular apex; msg = middle short gyrus; plg = posterior long gyrus; psg = posterior short gyrus;. Copyright Sanjiv Bhatia. Published with permission. Click here to view.

A large unilateral fronto-parieto-temporal scalp incision and craniotomy are performed centered on the perisylvian region (Fig. 3C). The lesser wing of the sphenoid is drilled to facilitate exposure of the sylvian fissure and obtain a flat access to the insular apex for insertion of depth electrodes (Fig. 3D). This is a very important step that should not be ignored.
FIG. 3.
FIG. 3.

Case 1. Technique of invasive monitoring. A: Preoperative MR image revealing cortical thickening of the right insula. B: The patient's head is positioned and rotated 45°. C: Large fronto-temporo-parietal craniotomy with drilling of the sphenoid wing. D: Visualization of the right hemisphere and superficial sylvian fissure. E: The superficial sylvian fissure is opened using standard microsurgical dissection. F: The deep sylvian fissure is dissected, thus exposing the MCA branches. G: The operculo-insular segments of the sylvian cistern are dissected, exposing the cortical surface of the insula. The inferior portion of the insula is exposed below the temporal opercula. H: After exposure of the superior insula until the superior insular sulcus, the posterior insula is exposed by splitting the deep portion of the posterior parietal and temporal opercula. I: An avascular portion of the insular apex is exposed. J and K: The insular depth electrode is placed through an avascular portion directed posterosuperiorly. L: Intraoperative photograph showing positioning of the subdural strip/grid electrodes. M: Ultrasound confirms positioning of the electrode within the insular cortex. N and O: Coregistered CT-MR images showing the position of the insular electrode. P: Scout image showing invasive electrodes. Figure is available in color online only.

Exposure and Electrode Implantation

Using the surgical microscope, the vertical ascending segment of the sylvian fissure is dissected and opened widely using standard microsurgical technique (Fig. 3E). An attempt is made to preserve the M3 arteries and veins. Exposure is performed in 3 steps. The ascending portion of the sylvian fissure is opened longitudinally. Sylvian fissure dissection should be started at the pars triangularis apex, as this is the largest opening of the superior sylvian fissure (Fig. 3F). Furthermore, opening the posterior ramus below the pars triangularis will expose the anterior/middle short gyri and anteroinferior insula, which lead down to the insular apex. The MCA branches are followed down to the deep portion of the fissure until the M2 branches overlying the insula are reached (Fig. 3G). At this stage, the deep operculo-insular fissure is dissected, exposing the inferior and then superior insula all the way to the inferior and superior sulci, respectively. The sylvian dissection may be carried out as far posteriorly as possible so that the entire extent of the insula can be exposed (Fig. 3H). This exposes the insular cortex beneath the opercula of the frontal, temporal, and parietal lobes. Finally, the relatively avascular insular apex and pole are exposed (Fig. 3I).36 The insular apex is the most prominent laterally projecting surface on the insula just above and behind the insular pole, the most anteroinferior point of the insula.

The insular depth electrode was then inserted starting at an avascular surface of the insular apex above the MCA branches after pial incision with a microblade (Fig. 3J and K). The electrode was directed posterosuperiorly to follow the sagittal axis of the insula, staying parallel to the insular cortex in the subpial region. Drilling down the lesser wing of sphenoid helps in holding the depth electrode in the direction of the insula prior to insertion. This can also be performed using ultrasound guidance (Fig. 3M). One 8-contact electrode was inserted in all but 1 case, in which two 4-contact electrodes were used. The electrodes (Spencer depth electrodes, Ad-Tech Medical Instrument Corp.) contain 8 contacts of 2.3 mm length separated by 5 mm from center to center. Papaverine (30 mg/ml) was instilled over the sylvian vessels to prevent spasm of the M2 and M3 vessels. Subdural grids and strips were then placed over the adjacent opercula and cortical convexities of the frontal, parietal, and temporal lobes based on the presurgical evaluation (Fig. 3L). The insular electrodes were sutured to the dura mater to prevent electrode migration. Additional depth electrodes were inserted in 1 patient into a frontal tuber. The electrodes were tunneled through the skin and sutured to the scalp with purse-string sutures to prevent postoperative cerebrospinal fluid leakage. The bone flap was replaced in all cases. Postoperative imaging was used to confirm the electrode position in all patients (Fig. 3N–P), and extraoperative video-EEG monitoring and functional mapping were performed in all patients.

Results

Patient Population

During the study period, 13 patients underwent invasive insular investigation for suspected insular-opercular/perisylvian refractory epilepsy. Of these, 2 patients were excluded as insular sampling was done without the transinsular apex electrodes: stereo-EEG was used in one patient and MR-guided transfrontal depth electrode placement in the other. Overall, 11 patients (5 boys) underwent invasive insular investigation with the transinsular apex depth electrode and perisylvian grids/strips for drug-resistant focal epilepsy of suspected insular/perisylvian origin (Table 1). The average age at surgery was 7.6 years (range 0.5–16.0 years).

TABLE 1.

Patient population undergoing insular investigation

Case No.Age (yrs), SexNo. of Insular ElectrodesNo. of Extrainsular ElectrodesGridStripNo. of Extrainsular Contacts & Cortical RegionsTotal No. of ContactsInitial Invasive Monitoring
DepthContactsDepthOrbitofrontalFrontoparietalTemporal NeocortexMesiotemporalInferior TemporalInterictalIctal
14, F2801103280048Rt posterior insulaRt posterior insula
213.5, F18012032293072Lt MTG, posteroinferior insulaLt MTG, posteroinferior insula
37, F18022448133682Lt ATL (STG, MTG, ITG), MTL of temporal pole behind prior resection, posterior insulaLt posterior insula, MTL/ATL of remaining temporal pole
46, F141 (in tuber)1203060040ECoG: rt frontal operculum & insulaECoG: no ictal events
50.5, M18013424240060Rt FO, PO, temporal neocortex (STG, MTG, ITG), insulaRt FO, temporal neocortex (STG, MTG, ITG), insula
68, F14012424140046Rt FO, TO, OF, & insulaRt insula
710, M1701243200043Lt OF, insulaLt OF, anteroinferior insula
88, F18014454184492Lt FO, PO, ATL (MTG, ITG), middle insulaLt ATL (ITG), anterior insula
98, M18011448120072Rt SMG of PL, posterior TO of STG & superior insulaNo Szs
1016, M18012445194080Rt PO, TORt insula, PO
112.5, M1421108240844Rt ATL (SMG, MTG, ITG), posterior insulaRt MTG & posterior insula
Mean7.61.16.81.51.122.534131.31.6
Min0.5141110800040
Max1628224454294892

ATL = anterior temporal lobe; FO = frontal operculum; ITG = inferior temporal gyrus; MTG = middle temporal gyrus; MTL = mesial temporal lobe; OF = orbitofrontal; PL = parietal lobe; PO = parietal operculum; SMG = supramarginal gyrus; STG = superior temporal gyrus; Sz = seizure; TO = temporal operculum.

Phase 1: Implantation: Electrodes and Safety

All 11 patients underwent invasive investigation, with 1 depth electrode directly implanted into the insula in 10 cases and 2 insular electrodes in 1 case (Table 1). Additional subdural grids and strips were placed to cover the suspected epileptogenic area of the perisylvian region (Fig. 2).

Postoperative imaging confirmed adequate placement of the electrodes in all cases (Fig. 3). Long-term monitoring confirmed localization of the epileptogenic focus to the insular lobe and various perisylvian regions in all cases (Fig 4). There were no invasive implantation procedure–related complications.

FIG. 4.
FIG. 4.

Case 6. Extraoperative long-term recording showing invasive electrode mapping, interictal and ictal seizure activity, proposed resection, and postresection MR image. iEEG = ictal EEG; iiEEG = interictal EEG. Figure is available in color online only.

Phase 2: Resection

All patients underwent subsequent insulectomy in addition to various degrees of concomitant cortical topectomy of the frontal, parietal, and temporal opercula in all patients. Four patients required repeat epilepsy surgery for persistent seizures, all of which included completion of insulectomy. Of these 4 patients, 1 underwent an additional insulectomy, 1 underwent insulectomy with concomitant fronto-opercular topectomy, and 2 patients underwent 2 additional procedures each (both of which included further completion of insular resection).

Discussion

In the early 1950s, Penfield and Faulk suggested that the insula may mimic temporal lobe seizures and could explain some failures following temporal lobe surgery.25 However, interest in insular lobe cortex epilepsy (ILE) and surgery was abandoned for almost half a century following Silfvenius' report that the addition of insulectomy to temporal lobe resection did not improve seizure control but increased surgical morbidity as a result of MCA vessel manipulation.32 The deep anatomical location of the insular cortex below the opercular cortices, combined with the dense sylvian vasculature that drapes over it, makes surgical treatment challenging and explains why neurosurgeons avoided invasive studies and resective surgery of the insula for a period of time. However, with advances in microsurgical and stereotactic techniques, there has been a renewed interest in insular surgery in adults over the past 30 years. Contemporary series have shown insular surgery to be both feasible and safe in adults,13,20 but there is limited evidence beyond a few reports in the pediatric literature. The goal of the current study was to demonstrate a new technique for invasive sampling of the insula, compare it to other techniques for invasive insular coverage, and discuss the role that insular sampling plays in focal drug-resistant extratemporal pediatric epilepsy.

When Should Insular-Opercular/Perisylvian Investigation Be Performed?

Intracranial electrode implantation with insular coverage is probably best reserved for pediatric patients with 1) early “insular/perisylvian” ictal manifestations in the context of nonlesional, drug-resistant temporal, parietal, or frontal lobe epilepsy based on noninvasive data; 2) lesional insular cases with discordant noninvasive presurgical data; 3) persisting disabling seizures following temporal, parietal, or frontal lobectomy; and 4) drug-resistant lesional temporal lobe epilepsy (TLE)/parietal lobe epilepsy (PLE)/frontal lobe epilepsy (FLE) with clinical and imaging features suggesting insular involvement. Whether drug-resistant, lesional TLE/PLE/FLE without clinical and imaging features suggesting insular involvement warrants invasive investigation during the initial surgery, or whether this should be withheld until after failed surgery, is still a matter of debate.15,16 Some authors advocate covering the insula in all cases of refractory TLE/PLE/FLE, but with this strategy only 10%–16% of patients have ILE and undergo subsequent insular resection.1,9,13 Some groups have reported higher rates of insular seizures (up to 37%) in patients undergoing insular sampling.33

Alternatively, surgery for ILE can be performed without invasive sampling. Intracranial electrode investigation was necessary in only about 19 (68%) pediatric ILE patients undergoing insulectomy in the literature.19,24,28,37 The remaining 32% of patients had lesional ILE as seen on MRI, and most went on to develop a good outcome (Engel Class I) following insular resection without long-term extraoperative intracranial recordings.37 In these lesional cases in which invasive monitoring with extraoperative monitoring is not performed, electrocorticography (ECoG) has been used to confirm involvement of the insula and map the epileptogenic area during surgery; this was done in 1 patient in this series.37 However, presurgical noninvasive studies have significant limitations, especially in children, and cannot always be used to reliably rule out ILE. Intraoperative ECoG should be reserved for cases with convergent clinical, radiological, and physiological noninvasive data. In children, young age and/or developmental and language delay render communication of initial/early subjective ictal symptoms (e.g., laryngeal discomfort) suboptimal in most cases.13 Also, insular epilepsy occurs in patients with nonlesional epilepsy and even patients with MRI lesions outside the insula.22,23,33 Insular epilepsy has been shown to coexist with independent extrainsular (e.g., temporal) epilepsy.33 Finally, lesions are often ill defined on MRI and may not give a reliable depiction of the extent of the epileptogenic zone, especially in children younger than 3 years.35 Several studies have shown that ictal or interictal scalp EEG has insufficient spatial resolution and cannot differentiate insular from overlying frontal, parietal, or temporal lobe epilepsy.15,16,23 Ictal SPECT and interictal PET rarely provide unequivocal evidence of ILE.16,33 Interestingly, magnetoencephalography has recently been shown to be superior to interictal PET and ictal SPECT in detecting ILE, although it is costly and is not available in most centers.21 The limitations of noninvasive presurgical evaluation in confirming ILE, combined with limited clinical information in children, has led some authors to advocate invasive monitoring with insular sampling in all suspected cases.13 The patients underwent insular placement of the depth electrode when there was a high clinical suspicion of insular onset. In our experience, the parasagittal transinsular apex depth electrode allowed confirmation of those suspicions and provided a guide to the extent of resection needed.

Options for Insular-Opercular Sampling

Previously described insular-opercular sampling methods include frame-based stereotactic methods1,15,16,27 and open microsurgical placement of orthogonally placed subpial insular depth electrodes in,33 or strip electrodes on,24 the insula following microsurgical opening of the sylvian fissure (Fig. 3, Table 2). Frame-based stereotactic techniques include the Talairach method, in which orthogonal electrodes are placed perpendicular to the sagittal plane using a Talairach stereotactic grid coregistered with angiography to avoid MCA branches.3,15,16,26 The Talairach method involves transopercular electrodes, which are placed through the opercula and into the insula, allowing recording from both the insula and the opercular cortex.3,15,16 Other newer stereo-EEG frame-based stereotactic insular depth electrodes include the transfrontal oblique electrode through the middle frontal gyrus (TFO),1,9,27,33 stereotactic TPO electrode through the inferior parietal lobule,1,27 and combined TFO-TPO methods.8

TABLE 2.

Review of techniques for insular sampling

Type of Technique & ElectrodeAdvantagesDisadvantagesAuthors & YearNo. of PtsCoverageNo. w/Insular Sz Involvement (%)No. of Insulectomies (%)No. of Complications (%)
No. of Insular Electrodes*No. of Insular Contacts*OnsetEarly PropagationRelated to Insular Depth ElectrodeRelated to Other Electrodes
Open/direct
Frameless
Transsylvian orthogonal depthAllows extensive ipsilateral hemispheric/opercular coverage; good medial & lateral insular coverage; electrode used as landmark during 2nd phase for subpial insular resectionWhen bilateral coverage is required; MCA vascular injury (hemiparesis), opercular retraction injury; lower contact/electrode ratio (n = 2) compared to oblique/parasagittal techniquesSurbeck et al., 201116Mean 3.5 (range 1–3)Mean 3.5 (range 1–6)7/19 (37)6/19 (32)2 (12.5) temporary: 1 foot drop from migration to internal capsule, 1 temporary dysphasia from opercular retraction3/16 (19) from subdural grids: 2 deficits from edema, 1 venous hemorrhage
Park et al., 20093343 (100)3 (100)NANA
Transsylvian stripAllows extensive ipsilateral hemispheric/opercular coverage; follows long axis of insula: high contact/electrode ratioMCA vascular injury (hemiparesis), retraction injury; limited coverage; bulky strip narrow spacePark et al., 20091121 (100)1 (100)00
Roper et al., 199311NS1 (100)1 (100)00
Frame-based
TPO depth electrodeNoneloquent corridor; avoids craniotomy, sylvian fissure dissection, opercular retraction; avoids passage through MCA & eloquent opercula; parietal; follows long axis of insula: high contact/electrode ratioWorse mediolateral insular coverage; limited anterior insula coverageAfif et al., 2008 (combined TPO, TFO)30Mean 1.2Mean 7.515 (50)5 (15)3 (10)0 (0)1 (3): intracerebral hemorrhage
Robles et al., 200991≥48 (89)1 (11)0 (0)0 (0)0
Park et al., 20092122 (100)2 (100)NANA
TFO depth electrodeSame as TPO except better w/suspected frontal focusWorse mediolateral coverage; limited posterior insula coverage; lower contact/electrode ratio than TPO approachAfif et al., 200830Mean 1.2Mean 7.515 (50)5 (15)3 (10)0 (0)1 (3): intracerebral hemorrhage
Desai et al., 201192029 totalMean 1.45 (range 1–2)2 (10)5 (25)0 (0)0 (0)1 misplaced electrode
Ryvlin et al., 200621Mean 6.5 (range 6–7)2 (100)0 (0)0 (0)00
Combined TFO/TPO`Combined advantages of TFO & TPOCombined disadvantages of TFO & TPOSurbeck et al., 201132Mean 8 (range 2–4 TFO, 5–7 TPO)7/19 (37)6/19 (32)00
OTO w/teleangiographyMost well established method; opercular coverage (involved in most adult cases of ILE); medial & lateral insular coverage; landmark for subpial insular resectionMCA vascular injury or sulcal injury; lower contact/electrode ratio (n = 2); lower insular coverage, particularly anteroinferior insula from overlying MCA; time consuming; less hemispheric coverageIsnard et al., 200021Mean 3.1 (range 2–5)NA2 (10)19 (90)0 (0)NANA
Isnard et al., 2004502.9NA5 (10)1 (2)2 (4)NANA
Dylgjeri et al., 201410Mean 4.3 (range 2–6)Mean 10 (range 5–16)10 (100)0 (0)10 (100)0 (0)0 (0)
Ryvlin et al., 20061121 (100)0 (0)0 (0)0 (0)0 (0)
Combined TFO/TPO/OTOCombined advantages of TPO, TFO, & OTOCombined disadvantages of TPO, TFO, & OTOProserpio et al., 20118NAMean 11 (range 2–31)8 (100)6/8 (75)0 (0)0 (0)
Blauwblomme et al., 201317Mean 1.3 (range 1–2)Mean 11 (range 4–18)2 (12)17 (100)0 (0)0 (0)1 (6): infection
Direct/open
Frameless
Transsylvian translimen parasagittalHemispheric/opercular coverage; follows long axis of insula: high contact-to-electrode ratioRequires craniotomy; opercular retraction; worse anteroinferior coverageCurrent study10 (ECoG in1)Mean 1.1 (range 1–2)Mean 7.1 (range 4–8)9 (90)0 (0)10 (100)0 (0)0 (0)

NA = not available; NS = not specified; pt = patient.

Number per patient, unless otherwise noted.

Efficacy/Coverage

Insular sampling with a parasagittal insular depth electrode through an open craniotomy combines the advantages of both the open direct transsylvian orthogonal method33 and stereo-EEG TFO/TPO methods,1 which provide excellent perisylvian/hemispheric coverage and good insular coverage, respectively (Fig. 2). Stereo-EEG techniques have gained in popularity over recent years. However, the ability to perform a wide coverage for epileptogenic zone and functional mapping is a vital differentiation, as the coverage and spatial resolution is greater with open techniques utilizing large grids than with stereo-EEG. The open techniques are thus favored when the suspected focus is thought to be both unilateral and either extending beyond the insula or involving the opercula/perisylvian structures and convexity, which is often the case in children.8,33 These techniques are particularly applicable in pediatric ILE, where the epileptogenic zone almost always involves cortex beyond the insula, typically the opercula or frontal/temporal cortex.13 The insertion point at the insular apex or pole and parasagittal orientation posterosuperiorly allow for extensive coverage along the length of the insula, from the most anterior short gyrus to the posterior long gyrus. However, our electrode was limited in its ability to cover the more anteroinferior portion of the insula (Figs. 1 and 3). The open parasagittal insular method has a similar contact-to-electrode ratio (average 6.8:1) to the TPO method, as both techniques follow the length of the insula. Coverage from these techniques is greater than that achieved with the TFO and orthogonally placed electrodes (open transsylvian or transopercular), which have a 5.2:1 and 2:1 contact-to-electrode ratio within the insula, respectively. The orthogonal techniques are limited because the insular gray matter is thin (< 5 mm),1 and they typically require additional electrodes to optimize coverage; however, they provide better mediolateral coverage than the oblique/parasagittal techniques.33

This study includes only 1 technique of insular sampling; thus, we cannot objectively compare or conclude on the relative efficiency of detecting insular seizures using other techniques, other than discussing the theoretical benefits and pitfalls of each technique. However, because interictal activity and ictal activity were detected in 10 and 9 of our 11 patients, respectively, this study suggests that this sampling method is an overall sensitive method for detecting insular seizures in well-selected candidates. The patients had a high suspicion of insular epilepsy based on the clinical semiology, electrophysiological changes, and failure of initial extrainsular surgery in some cases. The depth electrode provided a direct sampling of the insular cortex and confirmation of interictal/ictal onset, although most certainly it did not give a complete assessment of the spatial extent of its involvement.

An additional disadvantage of the orthogonal (open or stereotactic transopercular) technique is that electrode placement relies on insertion at avascular sites, which limits sampling of the insula due to the presence of the MCA vasculature, especially in the anteroinferior portion.36 The stereotactic transopercular technique allows simultaneous coverage of the frontal, temporal, and parietal opercula; however, some authors have found that insular depth recordings are contaminated by the presence of opercular waveforms.15,16 In our study, the opercula were investigated with subdural grid and strip electrodes as opposed to placing transopercular depth electrodes through the insula. These subdural strip/grids placed over the opercula have the advantage of greater spatial coverage than multiple transopercular depth electrodes and the potential of reduced risk of damaging the M3 MCA branches that wrap around the opercula. Finally, the parasagittal electrode along the length of the insula is an excellent landmark to guide safe second-stage subpial insular resection.

Electrode Safety

Our technique compares favorably to other open and stereo-EEG methods of insular sampling. Although the complication rate of the open method is reportedly higher than that of stereotactic techniques, including 12.5% and 19% rates of transient deficit related to the insular depth and subdural electrodes, respectively, there have been no permanent complications, suggesting its safety profile is acceptable.33 In our study, there were no transient or permanent complications related to placement of the insular depth electrode, sylvian fissure dissection, or concomitant subdural strip/grid electrode placement. However, edema, hemorrhage, and infection are well-documented risks associated with subdural electrodes, especially with an increasing number of electrodes used.33 Compared with the open orthogonal transsylvian technique described by Surbeck et al., the parasagittal implantation along the axis of the insula may help avoid migration into deeper neurological structures, such as the internal capsule or basal ganglia, which may result in transient hemiparesis.33 Although the open parasagittal insular electrode technique is more invasive than stereo-EEG, due to the requisite craniotomy, the associated risks may be mitigated by more accurate electrode placement, as the surgeon does not need to rely on stereotaxy. It does, however, mandate excellent knowledge of microsurgical anatomy and is associated with a learning curve. In addition, it facilitates brain mapping of eloquent cortex. The main concern with stereoEEG techniques is intracerebral hemorrhage, which has been reported to occur in up to 2.9% of cases, especially when multiple electrodes are used.7 Overall, stereo-EEG is associated with a 1%–2% severe morbidity of permanent deficit; however, this is based on studies utilizing a very high number of electrodes.6 There are no reported complications specifically caused by insular depth electrodes placed using stereo-EEG through TFO, TPO, or transopercular approaches.1,5,8–10,13,26,27,30

Conclusions

The parasagittal transinsular apex electrode is a feasible alterative to orthogonally placed open or oblique-placed stereotactic methods for sampling the insula. This method is safe and best suited for suspected unilateral cases with a suspected ictal onset zone extending beyond the insular cortex, as hemispheric grids and strips provide excellent coverage of these areas. The excellent hemispheric coverage and spatial resolution also allows for reliable brain mapping of eloquent cortex, which may be difficult with stereotactically placed depth electrodes.

Acknowledgments

We thank Benjamin Ellezam, MD, PhD, for his assistance in preparing the photos of the cadaveric specimen in the video.

References

  • 1

    Afif AChabardes SMinotti LKahane PHoffmann D: Safety and usefulness of insular depth electrodes implanted via an oblique approach in patients with epilepsy.. Neurosurgery 62:5 Suppl 2ONS471ONS4802008

  • 2

    Aghakhani YRosati ADubeau FOlivier AAndermann F: Patients with temporoparietal ictal symptoms and inferomesial EEG do not benefit from anterior temporal resection. Epilepsia 45:2302362004

  • 3

    Bancaud JTalairach J: [Methodology of stereo EEG exploration and surgical intervention in epilepsy.]. Rev Otoneuroophtalmol 45:3153281973. (Fr)

  • 4

    Barba CBarbati GMinotti LHoffmann DKahane P: Ictal clinical and scalp-EEG findings differentiating temporal lobe epilepsies from temporal ‘plus’ epilepsies. Brain 130:195719672007

  • 5

    Blauwblomme TDavid OMinotti LJob ASChassagnon SHoffman D: Prognostic value of insular lobe involvement in temporal lobe epilepsy: a stereoelectroencephalo-graphic study. Epilepsia 54:165816672013

  • 6

    Cossu MCardinale FCastana LCitterio AFrancione STassi L: Stereoelectroencephalography in the presurgical evaluation of focal epilepsy: a retrospective analysis of 215 procedures. Neurosurgery 57:7067182005

  • 7

    De Almeida ANOlivier AQuesney FDubeau FSavard GAndermann F: Efficacy of and morbidity associated with stereoelectroencephalography using computerized tomography—or magnetic resonance imaging-guided electrode implantation. J Neurosurg 104:4834872006

  • 8

    Desai ABekelis KDarcey TMRoberts DW: Surgical techniques for investigating the role of the insula in epilepsy: a review. Neurosurg Focus 32:3E62012

  • 9

    Desai AJobst BCThadani VMBujarski KAGilbert KDarcey TM: Stereotactic depth electrode investigation of the insula in the evaluation of medically intractable epilepsy. J Neurosurg 114:117611862011

  • 10

    Dobesberger JOrtler MUnterberger IWalser GFalkenstetter TBodner T: Successful surgical treatment of insular epilepsy with nocturnal hypermotor seizures. Epilepsia 49:1591622008

  • 11

    Duchowny MCross JH: Preoperative evaluation in children for epilepsy surgery. Handb Clin Neurol 108:8298392012

  • 12

    Duffau HCapelle LLopes MBitar ASichez JPvan Effenterre R: Medically intractable epilepsy from insular low-grade gliomas: improvement after an extended lesionectomy. Acta Neurochir (Wien) 144:5635732002

  • 13

    Dylgjeri STaussig DChipaux MLebas AFohlen MBulteau C: Insular and insulo-opercular epilepsy in childhood: an SEEG study. Seizure 23:3003082014

  • 14

    Guenot MIsnard J: [Epilepsy and insula.]. Neurochirurgie 54:3743812008. (Fr)

  • 15

    Isnard JGuénot MOstrowsky KSindou MMauguière F: The role of the insular cortex in temporal lobe epilepsy. Ann Neurol 48:6146232000

  • 16

    Isnard JGuénot MSindou MMauguière F: Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 45:107910902004

  • 17

    Isnard JMauguière F: [The insula in partial epilepsy.]. Rev Neurol (Paris) 161:17262005. (Fr)

  • 18

    Jayakar PGaillard WDTripathi MLibenson MHMathern GWCross JH: Diagnostic test utilization in evaluation for resective epilepsy surgery in children. Epilepsia 55:5075182014

  • 19

    Levitt MROjemann JGKuratani J: Insular epilepsy masquerading as multifocal cortical epilepsy as proven by depth electrode. J Neurosurg Pediatr 5:3653672010

  • 20

    Malak RBouthillier ACarmant LCossette PGiard NSaint-Hilaire JM: Microsurgery of epileptic foci in the insular region. J Neurosurg 110:115311632009

  • 21

    Mohamed ISGibbs SARobert MBouthillier ALeroux JMKhoa Nguyen D: The utility of magnetoencephalography in the presurgical evaluation of refractory insular epilepsy. Epilepsia 54:195019592013

  • 22

    Nguyen DKNguyen DBMalak RBouthillier A: Insular cortex epilepsy: an overview. Can J Neurol Sci 36:Suppl 2S58S622009

  • 23

    Nguyen DKNguyen DBMalak RLeroux JMCarmant LSaint-Hilaire JM: Revisiting the role of the insula in refractory partial epilepsy. Epilepsia 50:5105202009

  • 24

    Park YSLee YHShim KWLee YJKim HDLee JS: Insular epilepsy surgery under neuronavigation guidance using depth electrode. Childs Nerv Syst 25:5915972009

  • 25

    Penfield WFaulk ME Jr: The insula; further observations on its function. Brain 78:4454701955

  • 26

    Proserpio PCossu MFrancione STassi LMai RDidato G: Insular-opercular seizures manifesting with sleep-related paroxysmal motor behaviors: a stereo-EEG study. Epilepsia 52:178117912011

  • 27

    Robles SGGelisse PEl Fertit HTancu CDuffau HCrespel A: Parasagittal transinsular electrodes for stereo-EEG in temporal and insular lobe epilepsies. Stereotact Funct Neurosurg 87:3683782009

  • 28

    Roper SNLévesque MFSutherling WWEngel J Jr: Surgical treatment of partial epilepsy arising from the insular cortex. Report of two cases. J Neurosurg 79:2662691993

  • 29

    Ryvlin PKahane P: The hidden causes of surgery-resistant temporal lobe epilepsy: extratemporal or temporal plus?. Curr Opin Neurol 18:1251272005

  • 30

    Ryvlin PMinotti LDemarquay GHirsch EArzimanoglou AHoffman D: Nocturnal hypermotor seizures, suggesting frontal lobe epilepsy, can originate in the insula. Epilepsia 47:7557652006

  • 31

    Schofferman LZucherman JSchofferman JHsu KGunthorpe HPicetti G: Diptheroids and associated infections as a cause of failed instrument stabilization procedures in the lumbar spine. Spine (Phila Pa 1976) 16:3563581991

  • 32

    Silfvenius HGloor PRasmussen T: Evaluation of insular ablation in surgical treatment of temporal lobe epilepsy. Epilepsia 5:3073201964

  • 33

    Surbeck WBouthillier AWeil AGCrevier LCarmant LLortie A: The combination of subdural and depth electrodes for intracranial EEG investigation of suspected insular (perisylvian) epilepsy. Epilepsia 52:4584662011

  • 34

    Tanriover NRhoton AL JrKawashima MUlm AJYasuda A: Microsurgical anatomy of the insula and the sylvian fissure. J Neurosurg 100:8919222004

  • 35

    Taussig DDorfmüller GFohlen MJalin CBulteau CFerrand-Sorbets S: Invasive explorations in children younger than 3 years. Seizure 21:6316382012

  • 36

    Türe UYaşargil DCAl-Mefty OYaşargil MG: Topographic anatomy of the insular region. J Neurosurg 90:7207331999

  • 37

    von Lehe MWellmer JUrbach HSchramm JElger CEClusmann H: Insular lesionectomy for refractory epilepsy: management and outcome. Brain 132:104810562009

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Bhatia, Weil. Acquisition of data: Weil. Analysis and interpretation of data: Weil, Fallah. Drafting the article: Weil, Fallah. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Administrative/technical/material support: Weil.

Supplemental Information

Companion Papers

Weil AG, Le NMD, Jayakar P, Resnick T, Miller I, Fallah A, et al: Medically resistant pediatric insular-opercular/perisylvian epilepsy. Part 2: outcome following resective surgery. DOI: 10.3171/2016.4.PEDS15618.

Previous Presentations

This technique was presented at the Annual Epilepsy Surgery meeting in July 2014 in Gothenburg, Sweden.

Current Affiliations

  • Dr. Weil: Sainte Justine Hospital, University of Montreal, Canada.

  • Dr. Fallah: Department of Neurosurgery, David Geffen School of Medicine at the University of California, Los Angeles, CA.

  • Dr. Lewis: Division of Neurology, SickKids Hospital, Toronto, Ontario, Canada.

If the inline PDF is not rendering correctly, you can download the PDF file here.

Article Information

INCLUDE WHEN CITING Published online July 29, 2016; DOI: 10.3171/2016.4.PEDS15636.

Correspondence Sanjiv Bhatia, Department of Neurosurgery, Nicklaus Children's Hospital, 3100 Ambulatory Care Bldg., SW 62nd Ave., Miami, FL 33155. email: sanjiv.bhatia@mch.com.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Cadaveric brain with frontal, parietal, and temporal opercula removed demonstrating insular anatomy. Acc. = accessory; alg = anterior long gyrus; Ant. = anterior; Apex = insular apex; asg = anterior short gyrus; ins. = insular; Li = limen insulae; msg = middle short gyrus; plg = posterior long gyrus; psg = posterior short gyrus; Sup. = superior; Transv. = transverse.

  • View in gallery

    Medical illustration demonstrating the different techniques for insular sampling. Copyright Sanjiv Bhatia. Published with permission. SEEG = stereo-EEG.

  • View in gallery

    Case 1. Technique of invasive monitoring. A: Preoperative MR image revealing cortical thickening of the right insula. B: The patient's head is positioned and rotated 45°. C: Large fronto-temporo-parietal craniotomy with drilling of the sphenoid wing. D: Visualization of the right hemisphere and superficial sylvian fissure. E: The superficial sylvian fissure is opened using standard microsurgical dissection. F: The deep sylvian fissure is dissected, thus exposing the MCA branches. G: The operculo-insular segments of the sylvian cistern are dissected, exposing the cortical surface of the insula. The inferior portion of the insula is exposed below the temporal opercula. H: After exposure of the superior insula until the superior insular sulcus, the posterior insula is exposed by splitting the deep portion of the posterior parietal and temporal opercula. I: An avascular portion of the insular apex is exposed. J and K: The insular depth electrode is placed through an avascular portion directed posterosuperiorly. L: Intraoperative photograph showing positioning of the subdural strip/grid electrodes. M: Ultrasound confirms positioning of the electrode within the insular cortex. N and O: Coregistered CT-MR images showing the position of the insular electrode. P: Scout image showing invasive electrodes. Figure is available in color online only.

  • View in gallery

    Case 6. Extraoperative long-term recording showing invasive electrode mapping, interictal and ictal seizure activity, proposed resection, and postresection MR image. iEEG = ictal EEG; iiEEG = interictal EEG. Figure is available in color online only.

References

1

Afif AChabardes SMinotti LKahane PHoffmann D: Safety and usefulness of insular depth electrodes implanted via an oblique approach in patients with epilepsy.. Neurosurgery 62:5 Suppl 2ONS471ONS4802008

2

Aghakhani YRosati ADubeau FOlivier AAndermann F: Patients with temporoparietal ictal symptoms and inferomesial EEG do not benefit from anterior temporal resection. Epilepsia 45:2302362004

3

Bancaud JTalairach J: [Methodology of stereo EEG exploration and surgical intervention in epilepsy.]. Rev Otoneuroophtalmol 45:3153281973. (Fr)

4

Barba CBarbati GMinotti LHoffmann DKahane P: Ictal clinical and scalp-EEG findings differentiating temporal lobe epilepsies from temporal ‘plus’ epilepsies. Brain 130:195719672007

5

Blauwblomme TDavid OMinotti LJob ASChassagnon SHoffman D: Prognostic value of insular lobe involvement in temporal lobe epilepsy: a stereoelectroencephalo-graphic study. Epilepsia 54:165816672013

6

Cossu MCardinale FCastana LCitterio AFrancione STassi L: Stereoelectroencephalography in the presurgical evaluation of focal epilepsy: a retrospective analysis of 215 procedures. Neurosurgery 57:7067182005

7

De Almeida ANOlivier AQuesney FDubeau FSavard GAndermann F: Efficacy of and morbidity associated with stereoelectroencephalography using computerized tomography—or magnetic resonance imaging-guided electrode implantation. J Neurosurg 104:4834872006

8

Desai ABekelis KDarcey TMRoberts DW: Surgical techniques for investigating the role of the insula in epilepsy: a review. Neurosurg Focus 32:3E62012

9

Desai AJobst BCThadani VMBujarski KAGilbert KDarcey TM: Stereotactic depth electrode investigation of the insula in the evaluation of medically intractable epilepsy. J Neurosurg 114:117611862011

10

Dobesberger JOrtler MUnterberger IWalser GFalkenstetter TBodner T: Successful surgical treatment of insular epilepsy with nocturnal hypermotor seizures. Epilepsia 49:1591622008

11

Duchowny MCross JH: Preoperative evaluation in children for epilepsy surgery. Handb Clin Neurol 108:8298392012

12

Duffau HCapelle LLopes MBitar ASichez JPvan Effenterre R: Medically intractable epilepsy from insular low-grade gliomas: improvement after an extended lesionectomy. Acta Neurochir (Wien) 144:5635732002

13

Dylgjeri STaussig DChipaux MLebas AFohlen MBulteau C: Insular and insulo-opercular epilepsy in childhood: an SEEG study. Seizure 23:3003082014

14

Guenot MIsnard J: [Epilepsy and insula.]. Neurochirurgie 54:3743812008. (Fr)

15

Isnard JGuénot MOstrowsky KSindou MMauguière F: The role of the insular cortex in temporal lobe epilepsy. Ann Neurol 48:6146232000

16

Isnard JGuénot MSindou MMauguière F: Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 45:107910902004

17

Isnard JMauguière F: [The insula in partial epilepsy.]. Rev Neurol (Paris) 161:17262005. (Fr)

18

Jayakar PGaillard WDTripathi MLibenson MHMathern GWCross JH: Diagnostic test utilization in evaluation for resective epilepsy surgery in children. Epilepsia 55:5075182014

19

Levitt MROjemann JGKuratani J: Insular epilepsy masquerading as multifocal cortical epilepsy as proven by depth electrode. J Neurosurg Pediatr 5:3653672010

20

Malak RBouthillier ACarmant LCossette PGiard NSaint-Hilaire JM: Microsurgery of epileptic foci in the insular region. J Neurosurg 110:115311632009

21

Mohamed ISGibbs SARobert MBouthillier ALeroux JMKhoa Nguyen D: The utility of magnetoencephalography in the presurgical evaluation of refractory insular epilepsy. Epilepsia 54:195019592013

22

Nguyen DKNguyen DBMalak RBouthillier A: Insular cortex epilepsy: an overview. Can J Neurol Sci 36:Suppl 2S58S622009

23

Nguyen DKNguyen DBMalak RLeroux JMCarmant LSaint-Hilaire JM: Revisiting the role of the insula in refractory partial epilepsy. Epilepsia 50:5105202009

24

Park YSLee YHShim KWLee YJKim HDLee JS: Insular epilepsy surgery under neuronavigation guidance using depth electrode. Childs Nerv Syst 25:5915972009

25

Penfield WFaulk ME Jr: The insula; further observations on its function. Brain 78:4454701955

26

Proserpio PCossu MFrancione STassi LMai RDidato G: Insular-opercular seizures manifesting with sleep-related paroxysmal motor behaviors: a stereo-EEG study. Epilepsia 52:178117912011

27

Robles SGGelisse PEl Fertit HTancu CDuffau HCrespel A: Parasagittal transinsular electrodes for stereo-EEG in temporal and insular lobe epilepsies. Stereotact Funct Neurosurg 87:3683782009

28

Roper SNLévesque MFSutherling WWEngel J Jr: Surgical treatment of partial epilepsy arising from the insular cortex. Report of two cases. J Neurosurg 79:2662691993

29

Ryvlin PKahane P: The hidden causes of surgery-resistant temporal lobe epilepsy: extratemporal or temporal plus?. Curr Opin Neurol 18:1251272005

30

Ryvlin PMinotti LDemarquay GHirsch EArzimanoglou AHoffman D: Nocturnal hypermotor seizures, suggesting frontal lobe epilepsy, can originate in the insula. Epilepsia 47:7557652006

31

Schofferman LZucherman JSchofferman JHsu KGunthorpe HPicetti G: Diptheroids and associated infections as a cause of failed instrument stabilization procedures in the lumbar spine. Spine (Phila Pa 1976) 16:3563581991

32

Silfvenius HGloor PRasmussen T: Evaluation of insular ablation in surgical treatment of temporal lobe epilepsy. Epilepsia 5:3073201964

33

Surbeck WBouthillier AWeil AGCrevier LCarmant LLortie A: The combination of subdural and depth electrodes for intracranial EEG investigation of suspected insular (perisylvian) epilepsy. Epilepsia 52:4584662011

34

Tanriover NRhoton AL JrKawashima MUlm AJYasuda A: Microsurgical anatomy of the insula and the sylvian fissure. J Neurosurg 100:8919222004

35

Taussig DDorfmüller GFohlen MJalin CBulteau CFerrand-Sorbets S: Invasive explorations in children younger than 3 years. Seizure 21:6316382012

36

Türe UYaşargil DCAl-Mefty OYaşargil MG: Topographic anatomy of the insular region. J Neurosurg 90:7207331999

37

von Lehe MWellmer JUrbach HSchramm JElger CEClusmann H: Insular lesionectomy for refractory epilepsy: management and outcome. Brain 132:104810562009

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