Convergence of the arcuate fasciculus and third branch of the superior longitudinal fasciculus with direct cortical stimulation–induced speech arrest area in the anterior ventral precentral gyrus

J Neurosurg 139:1140–1151, 2023

The objective was to identify the correspondence between the anterior terminations of the arcuate fasciculus (AF) and third branch of the superior longitudinal fasciculus (SLF-III) and the intraoperative direct cortical electrical stimulation (DCS)–induced speech arrest area.

METHODS The authors retrospectively screened 75 glioma patients (group 1) who received intraoperative DCS mapping in the left dominant frontal cortex. To minimize the influence of tumors or edema, we subsequently selected 26 patients (group 2) with glioma or edema not affecting Broca’s area, the ventral precentral gyrus (vPCG), and the subcortical pathways to generate DCS functional maps and to construct the anterior terminations of AF and SLF-III with tractography. Next, a grid-by-grid pairwise comparison was performed between the fiber terminations and the DCS-induced speech arrest sites to calculate Cohen’s kappa coefficient (κ) in both groups 1 and 2. Finally, the authors also demonstrated the distribution of the AF/SLF-III anterior projection maps obtained in 192 healthy participants (group 3) and subsequently correlated these with the speech arrest sites in group 2 to examine their validity in predicting speech output area.

RESULTS The authors found that speech arrest sites were substantially consistent with SLF-III anterior terminations (group 1, κ = 0.64 ± 0.03; group 2, κ = 0.73 ± 0.05) and moderately consistent with AF (group 1, κ = 0.51 ± 0.03; group 2, κ = 0.49 ± 0.05) and AF/SLF-III complex (group 1, κ = 0.54 ± 0.03; group 2, κ = 0.56 ± 0.05) terminations (all p < 0.0001). The DCS speech arrest sites of the group 2 patients mainly (85.1%) emerged at the anterior bank of the vPCG (vPCGa). In group 3, both terminations of AF and SLF-III converged onto the vPCGa, and their terminations well predicted the DCS speech output area of group 2 (AF, area under the curve [AUC] 86.5%; SLF-III, AUC 79.0%; AF/SLF-III complex, AUC 86.7%).

CONCLUSIONS This study supports the key role of the left vPCGa as the speech output node by showing convergence between speech output mapping and anterior AF/SLF-III connectivity in the vPCGa. These findings may contribute to the understanding of speech networks and could have clinical implications in preoperative surgical planning.

Microsurgical anatomy and insular connectivity of the cerebral opercula

J Neurosurg 137:1509–1523, 2022

Radiological, anatomical, and electrophysiological studies have shown the insula and cerebral opercula to have extremely high functionality. Because of this complexity, interventions in this region cause higher morbidity compared to those in other areas of the brain. In most early studies of the insula and white matter pathways, insular dissection was begun after the opercula were removed. In this study, the authors examined the insula and deep white matter pathways to evaluate the insula as a whole with the surrounding opercula.

METHODS Twenty formalin-fixed adult cerebral hemispheres were studied using fiber microdissection techniques and examination of sectional anatomy. Dissections were performed from lateral to medial, medial to lateral, inferior to superior, and superior to inferior. A silicone brain model was used to show the normal gyral anatomy. Sections and fibers found at every stage of dissection were photographed with a professional camera. MRI tractography studies were used to aid understanding of the dissections.

RESULTS The relationships between the insula and cerebral opercula were investigated in detail through multiple dissections and sections. The relationship of the extreme and external capsules with the surrounding opercula and the fronto-occipital fasciculus with the fronto-orbital operculum was demonstrated. These findings were correlated with the tractography studies. Fibers of the extreme capsule connect the medial aspect of the opercula with the insula through the peri-insular sulcus. Medial to lateral dissections were followed with the removal of the central core structures, and in the last step, the medial surface of the cerebral opercula was evaluated in detail.

CONCLUSIONS This anatomical study clarifies our understanding of the insula and cerebral opercula, which have complex anatomical and functional networks. This study also brings a new perspective to the connection of the insula and cerebral opercula via the extreme and external capsules.

The nondecussating pathway of the dentatorubrothalamic tract in humans

The nondecussating pathway of the dentatorubrothalamic tract in humans

J Neurosurg 124:1406–1412, 2016

The dentatorubrothalamic tract (DRTT) is the major efferent cerebellar pathway arising from the dentate nucleus (DN) and decussating to the contralateral red nucleus (RN) and thalamus. Surprisingly, hemispheric cerebellar output influences bilateral limb movements. In animals, uncrossed projections from the DN to the ipsilateral RN and thalamus may explain this phenomenon. The aim of this study was to clarify the anatomy of the dentatorubrothalamic connections in humans.

Methods The authors applied advanced deterministic fiber tractography to a template of 488 subjects from the Human Connectome Project (Q1–Q3 release, WU-Minn HCP consortium) and validated the results with microsurgical dissection of cadaveric brains prepared according to Klingler’s method.

Results The authors identified the “classic” decussating DRTT and a corresponding nondecussating path (the nondecussating DRTT, nd-DRTT). Within each of these 2 tracts some fibers stop at the level of the RN, forming the dentatorubro tract and the nondecussating dentatorubro tract. The left nd-DRTT encompasses 21.7% of the tracts and 24.9% of the volume of the left superior cerebellar peduncle, and the right nd-DRTT encompasses 20.2% of the tracts and 28.4% of the volume of the right superior cerebellar peduncle.

Conclusions The connections of the DN with the RN and thalamus are bilateral, not ipsilateral only. This affords a potential anatomical substrate for bilateral limb motor effects originating in a single cerebellar hemisphere under physiological conditions, and for bilateral limb motor impairment in hemispheric cerebellar lesions such as ischemic stroke and hemorrhage, and after resection of hemispheric tumors and arteriovenous malformations. Furthermore, when a lesion is located on the course of the dentatorubrothalamic system, a careful preoperative tractographic analysis of the relationship of the DRTT, nd-DRTT, and the lesion should be performed in order to tailor the surgical approach properly and spare all bundles.

The lateral infratrigeminal transpontine window to deep pontine lesions

The lateral infratrigeminal transpontine window to deep pontine lesions

J Neurosurg 123:699–710, 2015

Surgery of brainstem lesions is increasingly performed despite the fact that surgical indications and techniques continue to be debated. The deep pons, in particular, continues to be a critical area in which the specific risks related to different surgical strategies continue to be examined. With the intention of bringing new knowledge into this important arena, the authors systematically examined the results of brainstem surgeries that have been performed through the lateral infratrigeminal transpontine window.

Methods Between 1990 and 2013, 29 consecutive patients underwent surgery through this window for either biopsy sampling or for removal of a deep pontine lesion. All of this work was performed at the Department of Neurosurgery of the Istituto Nazionale Neurologico “Carlo Besta”, in Milan, Italy. A retrospective analysis of the findings was conducted with the intention of bringing further clarity to this important surgical strategy.

Results The lateral infratrigeminal transpontine window was exposed through 4 different approaches: 1) classic retrosigmoid (15 cases), 2) minimally invasive keyhole retrosigmoid (10 cases), 3) translabyrinthine (1 case), and 4) combined petrosal (3 cases). No deaths occurred during the entire clinical study. The surgical complications that were observed included hydrocephalus (2 cases) and CSF leakage (1 case). In 6 (20.7%) of 29 patients the authors encountered new neurological deficits during the immediate postoperative period. All 6 of these patients had undergone lesion removal. In only 2 of these 6 patients were permanent sequelae observed at 3 months follow-up. These findings show that 93% of the patients studied did not report any permanent worsening of their neurological condition after this surgical intervention.

Conclusions This retrospective study supports the idea that the lateral infratrigeminal transpontine window is both a low-risk and safe corridor for either biopsy sampling or for removal of deep pontine lesions.

Fiber tractography of basal ganglia and cerebellum in PD

Fiber tractography of basal ganglia and cerebellum in PD

J Neurosurg 120:988–996, 2014

Stimulation of white matter pathways near targeted structures may contribute to therapeutic effects of deep brain stimulation (DBS) for patients with Parkinson disease (PD). Two tracts linking the basal ganglia and cerebellum have been described in primates: the subthalamopontocerebellar tract (SPCT) and the dentatothalamic tract (DTT). The authors used fiber tractography to evaluate white matter tracts that connect the cerebellum to the region of the basal ganglia in patients with PD who were candidates for DBS.

Methods. Fourteen patients with advanced PD underwent 3-T MRI, including 30-directional diffusion-weighted imaging sequences. Diffusion tensor tractography was performed using 2 regions of interest: ipsilateral subthalamic and red nuclei, and contralateral cerebellar hemisphere. Nine patients underwent subthalamic DBS, and the course of each tract was observed relative to the location of the most effective stimulation contact and the volume of tissue activated.

Results. In all patients 2 distinct tracts were identified that corresponded closely to the described anatomical features of the SPCT and DTT, respectively. The mean overall distance from the active contact to the DTT was 2.18 ± 0.35 mm, and the mean proportional distance relative to the volume of tissue activated was 1.35 ± 0.48. There was a nonsignificant trend toward better postoperative tremor control in patients with electrodes closer to the DTT.

Conclusions. The SPCT and the DTT may be related to the expression of symptoms in PD, and this may have implications for DBS targeting. The use of tractography to identify the DTT might assist with DBS targeting in the future.

Diffusion Tensor Imaging and Colored Fractional Anisotropy Mapping of the Ventralis Intermedius Nucleus of the Thalamus

Neurosurgery 69:1124–1130, 2011 DOI: 10.1227/NEU.0b013e3182296a42

The ventralis intermedius (VIM) nucleus of the thalamus is the primary surgical target for treatment of tremor. Most centers rely on indirect targeting based on atlas-defined coordinates rather than patient-specific anatomy, making intraoperative physiological mapping critical. Detailed identification of this target based on patientspecific anatomic features can help optimize the surgical treatment of tremor.

OBJECTIVE: To study colored fractional anisotropic images and diffusion tensor imaging (DTI) tractography to identify characteristic magnetic resonance appearances of the VIM nucleus.

METHODS: Four patients undergoing stereotactic surgery for essential tremor (ET) were retrospectively studied with analysis of magnetic resonance imaging-based colored fractional anisotropy (FA) images and fiber tractography. All were scanned with a 1.5-T magnetic resonance imaging unit, and all sequences were obtained before frame placement. Because the goal of this study was to identify the DTI characteristics of physiologically defined VIM nucleus, we selected and studied patients who had undergone DTI and had efficacious tremor control with intraoperative microlesioning effect and tremor reduction with less than 2.0-V stimulation.

RESULTS: Analysis of color FA maps, which graphically illustrate fiber directionality, revealed consistent anatomic patterns. The region of the VIM nucleus can be seen as an intermediate region where there is a characteristic transition of color. Presumptive VIM nucleus interconnectivity with sensorimotor cortex and cerebellum was identified via the internal capsule and the superior cerebellar peduncle, respectively. FA maps could also be used to distinguish segments of gray matter, white matter, and gray-white matter boundaries.

CONCLUSION: Analysis of DTI and FA maps on widely available 1.5-T magnetic resonance imaging yields clear identification of various structures key to neurosurgical targeting. Prospective evaluation of integrating DTI into neurosurgical planning may be warranted.

A role of diffusion tensor imaging in movement disorder surgery

Acta Neurochir DOI 10.1007/s00701-010-0742-2

The safe and reversible nature of deep brain stimulation (DBS) has allowed movement disorder neurosurgery to become commonplace throughout the world. Fundamental understanding of individual patient’s anatomy is critical for optimizing the effects and side effects of DBS surgery. Three patients undergoing stereotactic surgery for movement disorders, at the institution’s intraoperative magnetic resonance imaging operating suite, were studied with fiber tractography. Stereotactic targets and fiber tractography were determined on preoperative magnetic resonance imagings using the Schaltenbrand–Wahren atlas for definition in the BrainLab iPlan software (BrainLAB Inc., Feldkirchen, Germany). Subthalamic nucleus, globus pallidus interna, and ventral intermediate nucleus targets were studied. Diffusion tensor imaging parameters used ranged from 2 to 8 mm for volume of interest in the x/y/z planes, fiber length was kept constant at 30 mm, and fractional anisotropy threshold varied from 0.20 to 0.45. Diffusion tensor imaging tractography allowed reliable and reproducible visualization and correlation between frontal eye field, premotor, primary motor, and primary sensory cortices via corticospinal tracts and corticopontocerebellar tracts. There is an apparent increase in the number of cortical regions targeted by the fiber tracts as the region of interest is enlarged. This represents a possible mechanism of the increased effects and side effects observed with higher stimulation voltages. Currently available diffusion tensor imaging techniques allow potential methods to characterize the effects and side effects of DBS. This technology has the potential of being a powerful tool to optimize DBS neurosurgery