Microsurgical anatomy of the auditory radiations: revealing the enigmatic acoustic pathway from a surgical viewpoint.

OBJECTIVE: The thalamocortical projections of the auditory system have not been detailed via microanatomical fiber dissections from a surgical viewpoint. The aim of this study was to delineate the course of the auditory radiations (ARs) from the medial geniculate body to their final destination in the auditory cortex. The authors' additional purpose was to display the relevant neural structures in relation to their course en route to Heschl's gyrus. METHODS: White matter fibers were dissected layer by layer in a lateral-to-medial, inferolateral-to-superomedial, and inferior-to-superior fashion. RESULTS: The origin of ARs just distal to the medial geniculate body was revealed following the removal of the parahippocampal gyrus, cingulum bundle, and mesial temporal structures, in addition to the lateral geniculate body. Removing the fimbria, stria terminalis, and the tail of the caudate nucleus along the roof of the temporal horn in an inferior-to-superior direction exposed the lateral compartment of the sublenticular segment of the internal capsule as the predominant obstacle that prevents access to the ARs. The ARs were initially obscured by the inferolaterally located temporopulvinar tract of Arnold, and their initial course passed posterolateral to the temporopontine fascicle of Türck. The ARs subsequently traversed above the temporopulvinar fibers in a perpendicular manner and coursed in between the optic radiations at the sensory intersection region deep to the inferior limiting sulcus of insula. The distal part of the ARs intermingled with the fibers of the anterior commissure and inferior fronto-occipital fasciculus during its ascent toward Heschl's gyrus. The ARs finally projected to a large area over the superior temporal gyrus, extending well beyond the anteroposterior boundaries of the transverse temporal gyri. CONCLUSIONS: The ARs can be appreciated as a distinct fiber bundle ascending between the fibers of the sublenticular segment of the internal capsule and traversing superiorly along the roof of the temporal horn by spanning between the optic radiations. Our novel findings suggest potential disruption of the ARs' integrity during transsylvian and transtemporal approaches along the roof of the temporal horn toward the mesial temporal lobe. The detailed 3D understanding of the ARs' relations and awareness of their course may prove helpful to secure surgical interventions to the region.

The importance of preoperative planning to perform safely temporal lobe surgery.

Neurosurgeons should know the anatomy required for safe temporal lobe surgery approaches. The present study aimed to determine the angles and distances necessary to reach the temporal stem and temporal horn in surgical approaches for safe temporal lobe surgery by using a 3.0 T magnetic resonance imaging technique in post-mortem human brain hemispheres fixed by the Klingler method. In our study, 10 post-mortem human brain hemisphere specimens were fixed according to the Klingler method. Magnetic resonance images were obtained using a 3.0 T magnetic resonance imaging scanner after fixation. Surgical measurements were conducted for the temporal stem and temporal horn by magnetic resonance imaging, and dissection was then performed under a surgical microscope for the temporal stem. Each stage of dissection was achieved in high-quality three-dimensional images. The angles and distances to reach the temporal stem and temporal horn were measured in transcortical T1, trans-sulcal T1-2, transcortical T2, trans-sulcal T2-3, transcortical T3, and subtemporal trans-collateral sulcus approaches. The safe maximum posterior entry point for anterior temporal lobectomy was measured as 47.16 ± 5.00 mm. Major white-matter fibers in this region and their relations with each other are shown. The distances to the temporal stem and temporal horn, which are important in temporal lobe surgical interventions, were measured radiologically, and safe borders were determined. Surgical strategy and preoperative planning should consider the relationship of the lesion and white-matter pathways.

Transsylvian amygdalohippocampectomy for mesial temporal lobe epilepsy: Comparison of three different approaches.

OBJECTIVE: This study's objective was to compare the transinsular (TI-AH), transuncus (TU-AH), and temporopolar (TP-AH) amygdalohippocampectomy approaches regarding seizure control, temporal stem (TS) damage, and neurocognitive decline. METHODS: We included 114 consecutive patients with unilateral hippocampal sclerosis (HS) who underwent TI-AH, TU-AH, or TP-AH between 2002 and 2017. We evaluated seizure control using Engel classification. We used diffusion tensor imaging and postoperative Humphrey perimetry to assess the damage of the TS. We also performed pre- and postoperative memory performance and intelligence quotient (IQ). RESULTS: There were no significant differences in the proportion of patients free of disabling seizures (Engel IA+IB) among the three surgical approaches in the survival analysis. However, more patients were free of disabling seizures (Engel IA+IB) at 2 years of postsurgical follow-up with TP-AH (69.5%) and TI-AH (76.7%) as compared to the TU-AH (43.5%) approach (p = .03). The number of fibers of the inferior fronto-occipital fasciculus postoperatively was reduced in the TI-AH group compared with the TU-AH and TP-AH groups (p = .001). The rate of visual field defects was significantly higher with TI-AH (14/19, 74%) in comparison to the TU-AH (5/15, 33%) and TP-AH (13/40, 32.5%) approaches (p = .008). Finally, there was a significant postoperative decline in verbal memory in left-sided surgeries (p = .019) and delayed recall for both sides (p < .001) regardless of the surgical approach. However, TP-AH was the only group that showed a significant improvement in visual memory (p < .001) and IQ (p < .001) for both right- and left-sided surgeries. SIGNIFICANCE: The TP-AH group had better short-term seizure control than TU-AH, a lower rate of visual field defects than TI-AH, and improved visual memory and IQ compared to the other groups. Our findings suggest that TP-AH is a better surgical approach for temporal lobe epilepsy with HS than TI-AH and TU-AH.

Temporopolar amygdalohippocampectomy: seizure control and postoperative outcomes.

OBJECTIVE: The objective of this study was to evaluate the efficacy and safety of a modified surgical approach for the treatment of temporal lobe epilepsy secondary to hippocampal sclerosis (HS). This modified approach, called temporopolar amygdalohippocampectomy (TP-AH), includes a transsylvian resection of the temporal pole and subsequent amygdalohippocampectomy utilizing the limen insula as an anatomical landmark. METHODS: A total of 61 patients who were diagnosed with HS and underwent TP-AH between 2013 and 2017 were enrolled. Patients performed pre- and postoperative diffusion tensor imaging and were classified according to Engel's scale for seizure control. To evaluate the functional preservation of the temporal stem white-matter fiber tracts, the authors analyzed postoperative Humphrey perimetries and pre- and postoperative neurocognitive performance (Rey Auditory Verbal Learning Test [RAVLT], Weschler Memory Scale-Revised [WMS-R], intelligence quotient [IQ], Boston Naming Test [BNT], and semantic and phonemic fluency). Demographic data and surgical complications were also recorded and described. RESULTS: After a median follow-up of 36 ± 16 months, 46 patients (75.4%) achieved Engel class I, of whom 37 (60.6%) were Engel class IA. No significant changes in either the inferior frontooccipital fasciculus and optic radiation tractography were observed postoperatively for both left- and right-side surgeries. Reliable perimetry was obtained in 40 patients (65.6%), of whom 27 (67.5%) did not present any visual field defects (VFDs) attributable to surgery, while 12 patients (30%) presented with quadrant VFD, and 1 patient (2.5%) presented with hemifield VFD. Despite a significant decline in verbal memory (p = 0.007 for WMS-R, p = 0.02 for RAVLT recognition), there were significant improvements in both IQ (p < 0.001) and visual memory (p = 0.007). Semantic and phonemic fluency, and scores on the BNT, did not change postoperatively. CONCLUSIONS: TP-AH provided seizure control similar to historical temporal lobe approaches, with a tendency to preserve the temporal stem and a satisfactory incidence of VFD. Despite a significant decline in verbal memory, there were significant improvements in both IQ and visual memory, along with preservation of executive function. This approach can be considered a natural evolution of the selective transsylvian approach.

Temporal lobe structural evaluation after transsylvian selective amygdalohippocampectomy.

OBJECTIVE: Mesial temporal lobe epilepsy (MTLE) is the most common type of focal epilepsy in adolescents and adults, and in 65% of cases, it is related to hippocampal sclerosis (HS). Selective surgical approaches to the treatment of MTLE have as their main goal resection of the amygdala and hippocampus with minimal damage to the neocortex, temporal stem, and optic radiations (ORs). The object of this study was to evaluate late postoperative imaging findings on the temporal lobe from a structural point of view. METHODS: The authors conducted a retrospective evaluation of all patients with refractory MTLE who had undergone transsylvian selective amygdalohippocampectomy (SAH) in the period from 2002 to 2015. A surgical group was compared to a control group (i.e., adults with refractory MTLE with an indication for surgical treatment of epilepsy but who did not undergo the surgical procedure). The inferior frontooccipital fasciculus (IFOF), uncinate fasciculus (UF), and ORs were evaluated on diffusion tensor imaging analysis. The temporal pole neocortex was evaluated using T2 relaxometry. RESULTS: For the IFOF and UF, there was a decrease in anisotropy, voxels, and fibers in the surgical group compared with those in the control group (p < 0.001). An increase in relaxometry time in the surgical group compared to that in the control group (p < 0.001) was documented, suggesting gliosis and neuronal loss in the temporal pole. CONCLUSIONS: SAH techniques do not seem to totally preserve the temporal stem or even spare the neocortex of the temporal pole. Therefore, although the transsylvian approaches have been considered to be anatomically selective, there is evidence that the temporal pole neocortex suffers structural damage and potentially functional damage with these approaches.

The Caudate Nucleus: Its Connections, Surgical Implications, and Related Complications.

BACKGROUND: The caudate nucleus is a C-shaped structure that is located in the center of the brain and is divided into 3 parts: the head, body, and tail. METHODS: We detail the anatomic connections, relationships with other basal ganglia structures, and clinical implications of injury to the caudate nucleus. RESULTS: Anatomically, the most inferior transcapsular gray matter is the lentiform peduncle, which is the connection between the lentiform nucleus and caudate nucleus as well as the amygdala. The border between the tail and body of the caudate nucleus is the posterior insular point. The tail of the caudate nucleus is extraependymal in some parts and intraependymal in some parts of the roof of the temporal horn of the lateral ventricle. The tail of the caudate nucleus crosses the inferior limiting sulcus (temporal stem), and section of the tail during approaches to lesions involving the temporal stem may cause motor apraxia. The mean distance from the temporal limen point, which is the junction of the limen insula and inferior limiting sulcus, to the tail of the caudate nucleus in the temporal stem is 15.87 ± 3.10 mm. CONCLUSIONS: Understanding of the functional anatomy and connections of the distinct parts of the caudate nucleus is essential for deciding the extent of resection of lesions involving the caudate nucleus and the types of deficits that may be found postoperatively.

Enhancing outcomes of endoscopic vertical approach hemispherotomy: understanding the role of "temporal stem" residual connections causing recurrence of seizures.

OBJECTIVE: The authors sought to analyze the residual connections formed by the temporal stem as a cause for seizure recurrence following endoscopic vertical interhemispheric hemispherotomy and to review and compare lateral approach (perisylvian) with vertical approach surgical techniques to highlight the anatomical factors responsible for residual connections. METHODS: This study was a retrospective analysis of patients who underwent endoscopic hemispherotomy for drug-resistant epilepsy. Postoperative MR images were analyzed. Specific attention was given to anatomical 3D-acquired thin-section T1 images to assess the extent of disconnection, which was confirmed with a diffusion tensor imaging sequence. Cadaver brain dissection was done to analyze the anatomical factors responsible for persistent connections. RESULTS: Of 39 patients who underwent surgery, 80% (31/39) were seizure free (follow-up of 23.61 ± 8.25 months) following the first surgery. Thirty patients underwent postoperative MRI studies, which revealed persistent connections in 14 patients (11 temporal stem only; 3 temporal stem + amygdala + splenium). Eight of these 14 patients had persistent seizures. In 4 of these 8 patients, investigations revealed good concordance with the affected hemisphere, and repeat endoscopic disconnection of the residual connection was performed. Two of the 8 patients were lost to follow-up, and 2 had bihemispheric seizure onset. The 4 patients who underwent repeat endoscopic disconnection had seizure-free outcomes following the second surgery, increasing the good outcome total among all patients to 90% (35/39). Cadaveric brain dissection analysis revealed the anatomical factors responsible for the persistence of residual connections. CONCLUSIONS: In endoscopic vertical approach interhemispheric hemispherotomy (and also vertical approach parasagittal hemispherotomy) the temporal stem, which lies deep and parallel to the plane of disconnection, is prone to be missed, which might lead to persistent or recurrent seizures. The recognition of this limitation can lead to improved seizure outcome. The amygdala and splenium are areas less commonly prone to be missed during surgery.

Navigation-assisted trans-inferotemporal cortex selective amygdalohippocampectomy for mesial temporal lobe epilepsy; preserving the temporal stem.

OBJECTIVE: Selective amygdalohippocampectomy (SAH) can be used to obtain satisfactory seizure control in patients with mesial temporal lobe epilepsy (MTLE). Several SAH procedures have been reported to achieve satisfactory outcomes for seizure control, but none yield fully satisfactory outcomes for memory function. We hypothesized that preserving the temporal stem might play an important role. To preserve the temporal stem, we developed a minimally invasive surgical procedure, 'neuronavigation-assisted trans-inferotemporal cortex SAH' (TITC-SAH). METHODS: TITC-SAH was performed in 23 patients with MTLE (MTLE on the language-non-dominant hemisphere, n = 11). The inferior horn of the lateral ventricle was approached via the inferior or middle temporal gyrus along the inferior temporal sulcus under neuronavigation guidance. The hippocampus was dissected in a subpial manner and resected en bloc together with the parahippocampal gyrus. Seizure control at one year and memory function at 6 months postoperatively were evaluated. RESULTS: One year after TITC-SAH, 20 of the 23 patients were seizure-free (ILAE class 1), 2 were class 2, and 1 was class 3. Verbal memory improved significantly in 13 patients with a diagnosis of hippocampal sclerosis, for whom WMS-R scores were available both pre- and post-operatively. Improvements were seen regardless of whether the SAH was on the language-dominant or non-dominant hemisphere. No major complication was observed. CONCLUSION: Navigation-assisted TITC-SAH performed for MTLE offers a simple, minimally invasive procedure that appears to yield excellent outcomes in terms of seizure control and preservation of memory function, because this procedure does not damage the temporal stem. TITC-SAH should be one of the feasible surgical procedures for MTLE. ABBREVIATIONS: SAH: Amygdalohippocampectomy; MTLE: Mesial temporal lobe epilepsy (MTLE); TITC-SAH: Ttrans-inferotemporal cortex SAH; ILAE: International League Against Epilepsy (ILAE); MRI: Magnetic resonance imaging; EEG: Electroencephalography (EEG); FDG-PET: 8F-fluorodeoxyglucose (FDG)-positron emission tomography; ECoG: Electrocorticography; MEG: Magnetoencephalography; IMZ-SPECT: N-isopropyl-p(123I)-iodoamphetamine single photon emission computed tomography; WMS-R: Wechsler Memory Scale-Revised.

Clinical and Imaging Evaluation of Transuncus Selective Amygdalohippocampectomy.

BACKGROUND: Various reports have described the transuncus (TU) approach as a selective route to the amygdala and hippocampus, but this approach has not yet been submitted to solid postoperative imaging analysis. The objective of this study was to evaluate the anatomy, surgical technique, postoperative imaging analysis, and outcome in a series of patients with temporal lobe epilepsy who underwent selective amigdalohippocampectomy via a TU approach. METHODS: This was a prospective study of 25 consecutive patients who underwent selective amigdalohippocampectomy through a TU approach. The temporal stem and temporal pole were evaluated through different modalities of 3-Tesla magnetic resonance imaging, including tractography of optic radiation (OR), uncinate fascicle, and inferior fronto-occipital fascicle. Visual field analysis was performed with automated perimetry. RESULTS: The mean age was 40 ± 8.21 years, and mean follow-up was 26.44 + 12.58 months. Postoperatively, 21 patients (84%) were classified as Engel I (good seizure control). Diffusion tensor imaging (DTI) data showed that 78.2% of patients had some structural damage to the temporal stem and fibers of the uncinate fascicle were identified postoperatively in only 3 patients (13.04%). The inferior fronto-occipital fascicle was identified in 18 patients (78.3%); however, subsequent DTI analysis of the remaining fibers showed them to be damaged. Integrity of the OR did not differ between these 2 groups. CONCLUSIONS: A TU approach is a feasible and efficient approach to selective amigdalohippocampectomy for surgical treatment of temporal lobe epilepsy. Postoperative DTI analysis suggests that a TU approach results in more injury to the temporal stem and its associated white matter fiber tracts than expected by previous anatomic studies; however, it was efficient in preserving OR.

Microsurgical anatomy of the inferior limiting insular sulcus and the temporal stem.

OBJECT: The purpose of this study was to describe the location of each white matter pathway in the area between the inferior limiting insular sulcus (ILS) and temporal horn that may be crossed in approaches through the temporal stem to the medial temporal lobe. METHODS: The fiber tracts in 14 adult cadaveric cerebral hemispheres were examined using the Klingler technique. The fiber dissections were completed in a stepwise manner, identifying each white matter pathway in different planes and describing its position in relation to the anterior end of the ILS. RESULTS: The short-association fibers from the extreme capsule, which continue toward the operculae, are the most superficial subcortical layer deep to the ILS. The external capsule fibers are found deeper at an intermediate layer and are formed by the uncinate fasciculus, inferior frontooccipital fasciculus, and claustrocortical fibers in a sequential anteroposterior disposition. The anterior commissure forms the next deeper layer, and the optic radiations in the sublenticular part of the internal capsule represent the deepest layer. The uncinate fasciculus is found deep to the anterior third of the ILS, whereas the inferior frontooccipital fasciculus and optic radiations are found superficial and deep, respectively, at the posterior two-thirds of this length. CONCLUSIONS: The authors' findings suggest that in the transsylvian approach, a 6-mm incision beginning just posterior to the limen insula through the ILS will cross the uncinate fasciculus but not the inferior frontooccipital fasciculus or optic radiations, but that longer incisions carry a risk to language and visual functions.

Alterations of hippocampal projections in adult macaques with neonatal hippocampal lesions: a Diffusion Tensor Imaging study.

Neuropsychological and brain imaging studies have demonstrated persistent deficits in memory functions and structural changes after neonatal neurotoxic hippocampal lesion in monkeys. However, the relevant microstructural changes in the white matter of affected brain regions following this early insult remain unknown. This study assessed white matter integrity in the main hippocampal projections of adult macaque monkeys with neonatal hippocampal lesions, using diffusion tensor imaging (DTI). Data analysis was performed using tract-based spatial statistics (TBSS) and compared with volume of interest statistics. Alterations of fractional anisotropy (FA) and diffusivity indices were observed in fornix, temporal stem, ventromedial prefrontal cortex and optical radiations. To further validate the lesion effects on the prefrontal cortex, probabilistic diffusion tractography was used to examine the integrity of the fiber connections between hippocampus and ventromedial prefrontal cortex, and alterations were found in these connections. In addition, increased radial diffusivity in the left ventromedial prefrontal cortex correlated negatively with the severity of deficits in working memory in the same monkeys. The findings revealed microstructural changes due to neonatal hippocampal lesion, and confirmed that neonatal neurotoxic hippocampal lesions resulted in significant and enduring functional alterations in the hippocampal projection system.

A understanding of the temporal stem.

OBJECTIVE: There has been inconsistency about definition of the temporal stem despite of several descriptions demonstrating its microanatomy using fiber dissection and/or diffusion tensor tractography. This study was designed to clarify three dimensional configurations of the temporal stem. METHODS: The fronto-temporal regions of several formalin-fixed human cerebral hemispheres were dissected under an operating microscope using the fiber dissection technique. The consecutive coronal cuts of the dissected specimens were made to define the relationships of white matter tracts comprising the temporal stem and the subcortical gray matters (thalamus, caudate nucleus, amygdala) with inferior limiting (circular) sulcus of insula. RESULTS: The inferior limiting sulcus of insula, limen insulae, medial sylvian groove, and caudate nucleus/amygdala were more appropriate anatomical structures than the roof/dorso-lateral wall of the temporal horn and lateral geniculate body which were used to describe previously for delineating the temporal stem. The particular space located inside the line connecting the inferior limiting sulcus of insula, limen insulae, medial sylvian groove/amygdala, and tail of caudate nucleus could be documented. This space included the extreme capsule, uncinate fasciculus, inferior occipito-frontal fasciculus, anterior commissure, ansa peduncularis, and inferior thalamic peduncle including optic radiations, whereas the stria terminalis, cingulum, fimbria, and inferior longitudinal fiber of the temporal lobe were not passing through this space. Also, this continued posteriorly along the caudate nucleus and limiting sulcus of the insula. CONCLUSION: The temporal stem is white matter fibers passing through a particular space of the temporal lobe located inside the line connecting the inferior limiting sulcus of insula, limen insulae, medial sylvian groove/amygdala, and tail of caudate nucleus. The three dimensional configurations of the temporal stem are expected to give the very useful anatomical and surgical insights in the temporal lobe.