The arcuate fasciculus: Combining structure and function into surgical considerations.

BACKGROUND: Two Centuries from today, Karl Friedrich Burdach attributed the nomenclature "arcuate fasciculus" to a white matter (WM) pathway connecting the frontal to the temporal cortices by arching around the Sylvian fissure. Although this label remained essentially unvaried, the concepts related to it and the characterization of the structural properties of this bundle evolved along with the methodological progress of the past years. Concurrently, the functional relevance of the arcuate fasciculus (AF) classically restricted to the linguistic domain has extended to further cognitive abilities. These features make it a relevant structure to consider in a large variety of neurosurgical procedures. OBJECTIVE: Herein, we build on our previous review uncovering the connectivity provided by the Superior Longitudinal System, including the AF, and provide a handy representation of the structural organization of the AF by considering the frequency of defined reports in the literature. By adopting the same approach, we implement an account of which functions are mediated by this WM bundle. We highlight how this information can be transferred to the neurosurgical field by presenting four surgical cases of glioma resection requiring the evaluation of the relationship between the AF and the nearby structures, and the safest approaches to adopt. CONCLUSIONS: Our cumulative overview reports the most common wiring patterns and functional implications to be expected when approaching the study of the AF, while still considering seldom descriptions as an account of interindividual variability. Given its extension and the variety of cortical territories it reaches, the AF is a pivotal structure for different cognitive functions, and thorough understanding of its structural wiring and the functions it mediates is necessary for preserving the patient's cognitive abilities during glioma resection.

Microsurgical anatomy of the isthmic cingulum: a new white matter crossroad and neurosurgical implications in the posteromedial interhemispheric approaches and the glioma invasion patterns.

ABTRACT: The dichotomy of the cingulum bundle into the dorsal supracallosal and ventral parahippocampal parts is widely accepted; however, the retrosplenial component with its multiple alternative connections has not been revealed. The aim of this study was to delineate the microsurgical anatomy of a connectionally transition zone, the isthmic cingulum, in relation to the posteromedial interhemispheric access to the atrium and discuss the relevant patterns of glioma invasion on the basis of its fiber connections. White matter (WM) fibers were dissected layer by layer in a medial-to-lateral, lateral-to-medial, and posterior-to-anterior fashion. All related tracts and their connections were generated using deterministic tractography. The magnetic resonance imaging (MRI) tractography findings were correlated with those of fiber dissection. A medial parieto-occipital approach to reach the atrium was performed with special emphasis on the cingulate isthmus and underlying WM connections. The isthmic cingulum, introduced as a retrosplenial connectional crossroad for the first time, displayed multiple connections to the splenium and the superior thalamic radiations. Another new finding was the demonstration of lateral hemispheric extension of the isthmic cingulum fibers through the base of the posterior part of the precuneus at the base of the parieto-occipital sulcus. The laterally crossing cingulum fibers were interconnected with three distinct association tracts: the middle longitudinal (MdLF), the inferior frontooccipital fasciculi (IFOF), and the claustro-cortical fibers (CCF). In the process of entry to the atrium during posterior interhemispheric approaches, the splenial and thalamic connections, as well as the laterally crossing fibers of the isthmic cingulum, were all in jeopardy. The connectional anatomy of the retrosplenial area is much more complicated than previously known. The isthmic cingulum connections may explain the concept of interhemispheric and medial to lateral cerebral hemisphere invasion patterns in medial parieto-occipital and posteromesial temporal gliomas. The isthmic cingulum is of key importance in posteromedial interhemispheric approaches to both: the atrium and the posterior mesial temporal lobe.

Contribution of White Matter Fiber Bundle Damage to Language Change After Surgery for Temporal Lobe Epilepsy.

BACKGROUND AND OBJECTIVES: In medically refractory temporal lobe epilepsy (TLE), 30%-50% of patients experience substantial language decline after resection in the language-dominant hemisphere. In this study, we investigated the contribution of white matter fiber bundle damage to language change at 3 and 12 months after surgery. METHODS: We studied 127 patients who underwent TLE surgery from 2010 to 2019. Neuropsychological testing included picture naming, semantic fluency, and phonemic verbal fluency, performed preoperatively and 3 and 12 months postoperatively. Outcome was assessed using reliable change index (RCI; clinically significant decline) and change across timepoints (postoperative scores minus preoperative scores). Functional MRI was used to determine language lateralization. The arcuate fasciculus (AF), inferior fronto-occipital fasciculus (IFOF), inferior longitudinal fasciculus, middle longitudinal fasciculus (MLF), and uncinate fasciculus were mapped using diffusion MRI probabilistic tractography. Resection masks, drawn comparing coregistered preoperative and postoperative T1 MRI scans, were used as exclusion regions on preoperative tractography to estimate the percentage of preoperative tracts transected in surgery. Chi-squared assessments evaluated the occurrence of RCI-determined language decline. Independent sample t tests and MM-estimator robust regressions were used to assess the impact of clinical factors and fiber transection on RCI and change outcomes, respectively. RESULTS: Language-dominant and language-nondominant resections were treated separately for picture naming because postoperative outcomes were significantly different between these groups. In language-dominant hemisphere resections, greater surgical damage to the AF and IFOF was related to RCI decline at 3 months. Damage to the inferior frontal subfasciculus of the IFOF was related to change at 3 months. In language-nondominant hemisphere resections, increased MLF resection was associated with RCI decline at 3 months, and damage to the anterior subfasciculus was related to change at 3 months. Language-dominant and language-nondominant resections were treated as 1 cohort for semantic and phonemic fluency because there were no significant differences in postoperative decline between these groups. Postoperative seizure freedom was associated with an absence of significant language decline 12 months after surgery for semantic fluency. DISCUSSION: We demonstrate a relationship between fiber transection and naming decline after temporal lobe resection. Individualized surgical planning to spare white matter fiber bundles could help to preserve language function after surgery.

Accurate Preoperative Identification of Motor Speech Area as Termination of Arcuate Fasciculus Depicted by Q-Ball Imaging Tractography.

BACKGROUND: Tractography is one way to predict the distribution of cortical functional domains preoperatively. Diffusion tensor tractography (DTT) is commonly used in clinical practice, but is known to have limitations in delineating crossed fibers, which can be overcome by Q-ball imaging tractography (QBT). We aimed to compare the reliability of these 2 methods based on the spatial correlation between the arcuate fasciculus depicted by tractography and direct cortical stimulation during awake surgery. METHODS: In this study, 15 patients with glioma underwent awake surgery with direct cortical stimulation. Tractography was depicted in a three-dimensional computer graphic model preoperatively, which was integrated with a photograph of the actual brain cortex using our novel mixed-reality technology. The termination of the arcuate fasciculus depicted by either DTT or QBT and the results of direct cortical stimulation were compared, and sensitivity and specificity were calculated in speech-associated brain gyri: pars triangularis, pars opercularis, ventral precentral gyrus, and middle frontal gyrus. RESULTS: QBT had significantly better sensitivity and lower false-positive rate than DTT in the pars opercularis. The same trend was noted for the other gyri. CONCLUSIONS: QBT is more reliable than DTT in identification of the motor speech area and may be clinically useful in brain tumor surgery.

Revisiting Forel Field Surgery.

BACKGROUND: Lesioning the Forel field or the subthalamic region is considered a possible treatment for tremoric patients with Parkinson disease, essential tremor, and other diseases. This surgical treatment was performed in the 1960s to 1970s and was an alternative to thalamotomy. Recently, there has been increasing interest in the reappraisal of stimulating and/or lesioning these targets, partly as a result of innovations in imaging and noninvasive ablative technologies, such as magnetic resonance-guided focused ultrasonography. OBJECTIVE: We wanted to perform a thorough review of the subthalamic region, both from an anatomic and a surgical standpoint, to offer a comprehensive and updated analysis of the techniques and results reported for patients with tremor treated with different techniques. METHODS: We performed a systematic review of the literature, gathering articles that included patients who underwent ablative or stimulation surgical techniques, targeting the pallidothalamic pathways (pallidothalamic tractotomy), cerebellothalamic pathway (cerebellothalamic tractotomy), or subthalamic area. RESULTS: Pallidothalamic tractotomy consists of a reduced area that includes pallidofugal pathways. It may be considered an interesting target, given the benefit/risk ratio and the clinical effect, which, compared with pallidotomy, involves a lower risk of injury or involvement of vital structures such as the internal capsule or optic tract. Cerebellothalamic tractotomy and/or posterior subthalamic area are other alternative targets to thalamic stimulation or ablative surgery. CONCLUSIONS: Based on the significant breakthrough that magnetic resonance-guided focused ultrasonography has meant in the neurosurgical world, some classic targets such as the pallidothalamic tract, Forel field, and posterior subthalamic area may be reconsidered as surgical alternatives for patients with movement disorders.

Structural Brain Network Abnormalities and the Probability of Seizure Recurrence After Epilepsy Surgery.

OBJECTIVE: We assessed preoperative structural brain networks and clinical characteristics of patients with drug-resistant temporal lobe epilepsy (TLE) to identify correlates of postsurgical seizure recurrences. METHODS: We examined data from 51 patients with TLE who underwent anterior temporal lobe resection (ATLR) and 29 healthy controls. For each patient, using the preoperative structural, diffusion, and postoperative structural MRI, we generated 2 networks: presurgery network and surgically spared network. Standardizing these networks with respect to controls, we determined the number of abnormal nodes before surgery and expected to be spared by surgery. We incorporated these 2 abnormality measures and 13 commonly acquired clinical data from each patient into a robust machine learning framework to estimate patient-specific chances of seizures persisting after surgery. RESULTS: Patients with more abnormal nodes had a lower chance of complete seizure freedom at 1 year and, even if seizure-free at 1 year, were more likely to relapse within 5 years. The number of abnormal nodes was greater and their locations more widespread in the surgically spared networks of patients with poor outcome than in patients with good outcome. We achieved an area under the curve of 0.84 ± 0.06 and specificity of 0.89 ± 0.09 in predicting unsuccessful seizure outcomes (International League Against Epilepsy [ILAE] 3-5) as opposed to complete seizure freedom (ILAE 1) at 1 year. Moreover, the model-predicted likelihood of seizure relapse was significantly correlated with the grade of surgical outcome at year 1 and associated with relapses up to 5 years after surgery. CONCLUSION: Node abnormality offers a personalized, noninvasive marker that can be combined with clinical data to better estimate the chances of seizure freedom at 1 year and subsequent relapse up to 5 years after ATLR. CLASSIFICATION OF EVIDENCE: This study provides Class II evidence that node abnormality predicts postsurgical seizure recurrence.

Functional tracts of the cerebellum-essentials for the neurosurgeon.

The cerebellum is historically implicated in motor coordination, but accumulating modern evidence indicates involvement in non-motor domains, including cognition, emotion, and language. This correlates with the symptoms observed in postoperative cerebellar mutism syndrome (CMS). Profound knowledge of cerebellar functional topography and tractography is important when approaching cerebellar tumors, as surgical trauma to relevant structures of cerebellar pathways plays a role in the pathogenesis of CMS. The aim of this systematic review is to provide a concise overview of relevant modern neuroimaging data and cerebellar functional tracts with regard to neurosurgical procedures.

Augmented reality for the virtual dissection of white matter pathways.

BACKGROUND: The human white matter pathway network is complex and of critical importance for functionality. Thus, learning and understanding white matter tract anatomy is important for the training of neuroscientists and neurosurgeons. The study aims to test and evaluate a new method for fiber dissection using augmented reality (AR) in a group which is experienced in cadaver white matter dissection courses and in vivo tractography. METHODS: Fifteen neurosurgeons, neurolinguists, and neuroscientists participated in this questionnaire-based study. We presented five cases of patients with left-sided perisylvian gliomas who underwent awake craniotomy. Diffusion tensor imaging fiber tracking (DTI FT) was performed and the language-related networks were visualized separated in different tracts by color. Participants were able to virtually dissect the prepared DTI FTs using a spatial computer and AR goggles. The application was evaluated through a questionnaire with answers from 0 (minimum) to 10 (maximum). RESULTS: Participants rated the overall experience of AR fiber dissection with a median of 8 points (mean ± standard deviation 8.5 ± 1.4). Usefulness for fiber dissection courses and education in general was rated with 8 (8.3 ± 1.4) and 8 (8.1 ± 1.5) points, respectively. Educational value was expected to be high for several target audiences (student: median 9, 8.6 ± 1.4; resident: 9, 8.5 ± 1.8; surgeon: 9, 8.2 ± 2.4; scientist: 8.5, 8.0 ± 2.4). Even clinical application of AR fiber dissection was expected to be of value with a median of 7 points (7.0 ± 2.5). CONCLUSION: The present evaluation of this first application of AR for fiber dissection shows a throughout positive evaluation for educational purposes.

Surgical Treatment for the Cluster Headache: Clinical Experience.

BACKGROUND: Cluster headache (CH) refers to the most painful primary headache that sometimes leads to poor quality of life and associated disability. So far, no treatment has been found to cure CHs. In this study, we introduce a novel and effective surgery for CH. METHODS: We studied 6 patients with CH diagnosed according to the criteria of the Headache Classification Committee of the IHS, third edition, who were eligible for surgical treatment on the basis of strong requirements. All of them underwent temporal craniectomy and transection of the greater superficial petrosal nerve and deep petrosal nerve pathway to the sphenopalatine ganglion. RESULTS: All 6 patients had the surgery for CH and follow-up per 3 months. We significantly cured their pain and autonomic dysfunction. In the follow-up process none of the patients had reoccurring alacrimia. All of them had reduction of secretion of nasal, oral mucosa, and parotid and were satisfied with the surgery. CONCLUSIONS: All 6 patients with CH received surgery by transection greater superficial petrosal nerve and deep petrosal nerve pathway to the sphenopalatine ganglion and were completely cured, and adverse events and serious complications did not occur.

Disconnection of the perirhinal and insular cortices severely disrupts taste neophobia.

It is well known that the perirhinal (Prh) and insular (IC) cortices are reciprocally connected, mainly through ipsilateral projections. Although some studies have demonstrated that excitotoxic lesions to these regions, each separately, disrupt taste neophobia, it is not yet known whether the two regions have functional interactions with one another. To find out if they form a functional unit, we examined the effects of crossed excitotoxic lesions to the Prh and the contralateral IC (contralateral group). This group's performance was compared to that of rats with ipsilateral Prh and IC lesions (ipsilateral group) and to that of control-operated rats. All the animals received a 0.3% saccharin solution for fifteen minutes on five consecutive days. Rats with contralateral Prh-IC lesions drank significantly higher amounts of saccharin than the other groups during the first encounter with the novel taste, indicating a disruption in neophobia. However, the lesions did not disrupt attenuation of neophobia, with the contralateral group reaching asymptote in trial 2 and the rest of the groups after 3-5 days of exposure to the saccharin. These findings suggest that both Prh and IC play a necessary role in taste neophobia. Additionally, the two cortices function interdependently and their interaction is critical for normal expression of taste neophobia.

Evaluation of Ideal Extent of Corpus Callosotomy Based on the Location of Intracallosal Motor Fibers.

BACKGROUND: The corpus callosotomy (CCT) has been reported as an effective procedure to alleviate drop attacks. However, the extent of CCT remains debatable. Classical studies suggest that motor fibers traverse mainly through the anterior half of the corpus callosum (CC), although recent diffusion tensor imaging studies described that motor fibers crossed the CC in a more posterior location, emphasizing the posterior midbody and the isthmus. METHODS: Cortical and subcortical structures were examined in 30 hemispheres prepared for white matter fiber dissection. Dissections were carried out under surgical magnification to trace fibers originating from the primary motor cortex and their course through the CC. The distance of the most anterior and posterior motor fibers to the tip of the genu were measured, and the extent of CCT enabling disconnection of all motor fibers was calculated. RESULTS: Motor fibers coursed through the posterior half of the CC in the majority of hemispheres, mainly locating in posterior midbody and the isthmus. Callosal fibers should be interrupted to an average of 61% ± 0.07% point of the CC to reach the anterior limit of motor fibers and to an average of 69% ± 0.07% point to include posterior limit of motor fibers. Motor fibers were extending until the posterior one third of the CC in 22 specimens. CONCLUSIONS: Anterior-half CCT did not include all motor fibers in any specimen. Anterior two thirds CCT disrupted all motor fibers in one fourth of the cases. Our findings suggest that an ideal CCT should extend to the posterior midbody and isthmus of the CC.

History of the Network Approach in Epilepsy Surgery.

We provide a history and overview of the network approach to epilepsy surgery. Models of the epileptogenic zone (EZ) have evolved considerably over the years with more recent models accounting for the connectivity and network properties of epileptic foci. Next, we describe several examples of network phenotypes of focal epilepsy and how these have the potential to influence surgical decision-making and patient outcome. Future research will provide new insight into how network models of the EZ can determine optimal surgical interventions that improve seizure outcomes and optimize cognitive outcomes.

Epileptogenic Network Formation.

Epilepsy is characterized by specific alterations in network organization. The main parameters at the basis of epileptogenic network formation are alterations of cortical thickness, development of pathologic hubs, modification of hub distribution, and white matter alterations. The effect is a reinforcement of brain connectivity in both the epileptogenic zone and the propagation zone. Moreover, the epileptogenic network is characterized by some specific neurophysiologic biomarkers that evidence the tendency of the network itself to shift from an interictal state to an ictal one. The recognition of these features is crucial in planning epilepsy surgery.

Extracranial Interictal and Ictal EEG in sEEG Planning.

Analysis of scalp electroencephalogram (EEG) findings is indispensable to investigation of epilepsy surgery candidates. Maxima of slowing and epileptiform spiking on interictal EEG reflect gross localization of core epileptogenic regions within a network. Important negative scalp EEG findings are those associated with deep foci. Ictal EEG is important in confirming concordance with interictal EEG and other ancillary data. Generalized interictal and ictal EEG findings may occur in epilepsies that are otherwise focal. Detailed individual analyses of scalp EEG features are prelude to a more global synthesis, whose coherence in suggesting plausible network hypothesis presage a subsequently successful scalp EEG evaluation.

Functional Networks in Epilepsy Presurgical Evaluation.

Continuing advancements in neuroimaging methodology allow for increasingly detailed in vivo characterization of structural and functional brain networks, leading to the recognition of epilepsy as a disorder of large-scale networks. In surgical candidates, analysis of functional networks has proved invaluable for the identification of eloquent brain areas, such as hemispherical language dominance. More recently, connectome-based biomarkers have demonstrated potential to further inform clinical decision making in drug-refractory epilepsy. This article summarizes current evidence on epilepsy as a network disorder, emphasizing potential benefits of network analysis techniques for preoperative assessments and resection planning.

Epileptogenicity Mapping: A Quantitative Approach to Identify the Seizure Onset.

During the presurgical evaluation of patients with focal refractory epilepsies, the spatial mapping of the seizure onset zone (SOZ) and seizure propagation networks critically depends on the use of different features extracted from the intracranial electroencephalogram (IEEG). The identification of the SOZ is usually based on visual inspection by highly qualified neurophysiologists. However, quantitative IEEG analyses have recently been developed by exploiting signal and image characteristics in order to improve and expedite the SOZ detection. Here, the authors briefly review some of the latest methods proposed by different research groups and then present the recent implementation in Brainstorm software.

Decision Making in Epilepsy Surgery.

The need to emphasize the network concept arises from the fact that the traditional surgical philosophy in American epilepsy centers has prioritized an electrical-anatomic, focus-oriented approach. In contrast, the stereoelectroencephalography philosophy focuses on using electrophysiology to determine the regions of cortex generating the clinical manifestation of the seizure. Viewing epilepsy surgery as network surgery enables optimal consideration of decisions related to the need for and method of intracranial monitoring, potential role of subcortical structures in seizure organization and propagation, upfront use of combinatorial therapies to prevent seizure emergence from the network, and use of neuromodulation in novel epilepsy indications.

Direct evidence of the relationship between brain metastatic adenocarcinoma and white matter fibers: A fiber dissection and diffusion tensor imaging tractography study.

It is commonly known that brain metastases usually have clear boundaries in magnetic resonance imaging. However, little is known regarding the trajectory of white matter fibers around the tumors, especially using the fiber dissection technique. Here, we focused on the anatomical interaction between white matter fibers and the tumor, using the fiber dissection in a postmortem brain with metastatic tumor and compared the findings with those of diffusion tensor imaging (DTI) tractography. One postmortem human brain hemisphere with metastatic adenocarcinoma in the Broca's area was dissected using fiber dissection following the Klingler's method. In order to compare the in vitro and in vivo results, additional brains from 15 patients with metastatic adenocarcinomas, the volumes of which were comparable to that of the adenocarcinoma in the brain used for fiber dissection, were analyzed using DTI tractographic reconstruction. Morphological findings of white matter bundles running around the tumor were compared between the two techniques. In the fiber dissection technique, the superior longitudinal fascicle, arcuate fascicle, and frontal aslant tract could be dissected, and the white matter bundles were curved and retracted to avoid the tumor. In all the cases analyzed, white matter fibers or streamlines surrounding the tumor avoided the lesion. Using the fiber dissection technique, this is the first direct evidence to elucidate the anatomy of white matter fibers affected by a metastatic brain. This suggests that brain metastatic adenocarcinoma is an intra-axial neoplasm with extra-axial white matter structures.

Advanced Imaging and Direct Targeting of the Motor Thalamus and Dentato-Rubro-Thalamic Tract for Tremor: A Systematic Review.

Direct targeting methods for stereotactic neurosurgery in the treatment of essential tremor have been the subject of active research over the past decade but have not yet been systematically reviewed. We present a clinically oriented topic review based on Preferred Reporting Items for Systematic Reviews and Meta-Analyses Group guidelines. Our focus is studies using advanced magnetic resonance imaging (MRI) techniques (ultrahigh-field structural MRI, diffusion-weighted imaging, diffusion-tensor tractography, and functional MRI) for patient specific, in vivo identification of the ventral intermediate nucleus and the dentato-rubro-thalamic tract.

Resting-State Functional Connectome in Patients with Brain Tumors Before and After Surgical Resection.

PURPOSE: High-grade glioma surgery has evolved around the principal belief that a safe maximal tumor resection improves symptoms, quality of life, and survival. Mapping brain function has been recently improved by resting-state functional magnetic resonance imaging (rest-fMRI), a novel imaging technique that explores networks connectivity at "rest." METHODS: This prospective study analyzed 10 patients with high-grade glioma in whom rest-fMRI connectivity was assessed both in single-subject and in group analysis before and after surgery. Seed-based functional connectivity analysis was performed with CONN toolbox. Network identification focused on 8 major functional connectivity networks. A voxel-wise region of interest (ROI) to ROI correlation map to assess functional connectivity throughout the whole brain was computed from a priori seeds ROI in specific resting-state networks before and after surgical resection in each patient. RESULTS: Reliable topography of all 8 resting-state networks was successfully identified in each participant before surgical resection. Single-subject functional connectivity analysis showed functional disconnection for dorsal attention and salience networks, whereas the language network demonstrated functional connection either in the case of left temporal glioblastoma. Functional connectivity in group analysis showed wide variations of functional connectivity in the default mode, salience, and sensorimotor networks. However, salience and language networks, salience and default mode networks, and salience and sensorimotor networks showed a significant correlation (P uncorrected <0.0025; P false discovery rate <0.077) in comparison before and after surgery confirming non-disconnection of these networks. CONCLUSIONS: Resting-state fMRI can reliably detect common functional connectivity networks in patients with glioma and has the potential to anticipate network alterations after surgical resection.