Altered corticospinal microstructure and motor cortex excitability in gliomas: an advanced tractography and transcranial magnetic stimulation study

Abstract

OBJECTIVEThis prospective case-control study was conducted to examine whether spherical deconvolution (SD) can unveil microstructural abnormalities in the corticospinal tract (CST) caused by IDH-mutant gliomas. To determine the significance of abnormal microstructure, the authors investigated the correlation between diffusion parameters and neurophysiological data collected with navigated transcranial magnetic stimulation (nTMS).METHODSTwenty participants (10 patients and 10 healthy controls) were recruited. Diffusion-weighted images were acquired on a 3-T MRI scanner using a cardiac-gated single-shot spin echo echo-planar imaging multiband sequence (TE 80 msec, TR 4000 msec) along 90 diffusion directions with a b-value of 2500 sec/mm2 (FOV 256 × 256 mm). Diffusion tensor imaging tractography and SD tractography were performed with deterministic tracking. The anterior portion of the ipsilateral superior peduncle and the precentral gyrus were used as regions of interest to delineate the CST. Diffusion indices were extracted and analyzed for significant differences between hemispheres in patients and between patient and control groups. A navigated brain stimulation system was used to deliver TMS pulses at hotspots at which motor evoked potentials (MEPs) for the abductor pollicis brevis, first digital interosseous, and abductor digiti minimi muscles are best elicited in patients and healthy controls. Functional measurements such as resting motor threshold (rMT), amplitude of MEPs, and latency of MEPs were noted. Significant differences between hemispheres in patients and between patients and controls were statistically analyzed. The Spearman rank correlation was used to investigate correlations between diffusion indices and functional measurements.RESULTSThe hindrance modulated orientational anisotropy (HMOA), measured with SD tractography, is lower in the hemisphere ipsilateral to glioma (p = 0.028). The rMT in the hemisphere ipsilateral to a glioma is significantly greater than that in the contralateral hemisphere (p = 0.038). All measurements contralateral to the glioma, except for the mean amplitude of MEPs (p = 0.001), are similar to those of healthy controls. Mean diffusivity and axial diffusivity from SD tractography are positively correlated with rMT in the hemisphere ipsilateral to glioma (p = 0.02 and 0.006, respectively). The interhemispheric difference in HMOA and rMT is correlated in glioma patients (p = 0.007).CONCLUSIONSSD tractography can demonstrate microstructural abnormality within the CST of patients with IDH1-mutant gliomas that correlates to the functional abnormality measured with nTMS.

White matter variability, cognition, and disorders: a systematic review

“…This multi-modal brain mapping approach is able to reveal variation but also ‘atypical cases’, meaning the patients that do not fit expected assumptions of associations between brain areas or connections and deficit in certain cognitive domains. In the surgical setting, transcranial magnetic stimulation for presurgical planning (e.g., Giampiccolo et al 2020 ; Mirchandani et al 2020 ), deep brain stimulation (e.g., Calabrese 2016 ; Akram et al 2017 ), and direct electrical cortical stimulation during awake surgery (e.g., Puglisi et al 2019 ; Middlebrooks et al 2020 ) have been aided by the consideration of inter-individual variability in white matter tracts estimated with tractography. However, there has not yet been a systematic attempt to capture this variability in connections across the entire brain and associate white matter phenotypes with cognitive profiles and clinical dimensions.…”

Minimally invasive approach to a deep-seated motor eloquent brain tumour: a technical note

“…Preoperative and intraoperative functional mapping has been widely described in resection surgery of infiltrative gliomas to preserve functional integrity and this has shown to improve long-term outcomes [ 10–14 ]. In this case, the preoperative nTMS documented a functional impairment of the primary motor cortex and CST and tractography revealed altered white matter microstructure of the CST [ 15 ]. This information was important as it indicated an injured motor pathway more susceptible to non-reversible injury [ 16 ].…”

Impaired phase synchronization of motor‐evoked potentials reflects the degree of motor dysfunction in the lesioned human brain

“…While corticospinal conduction varies physiologically due to fluctuations of cortical (Khademi, Royter, & Gharabaghi, 2018; Naros, Lehnertz, Leão, Ziemann, & Gharabaghi, 2020) and spinal excitability (van Elswijk et al, 2010; Naros et al, 2020), lesions within the corticospinal system (e.g., brain tumors) can cause additional impairment of CSV transmission (Cirillo, Calabro, & Perez, 2016; Hallett, 2000; Kobayashi & Pascual‐Leone, 2003; Stinear et al, 2007). However, conventional MEP characteristics (i.e., latency and amplitude) are often ambiguous, resulting in an inconsistency between clinical (e.g., motor impairment) and electrophysiological findings (Machetanz et al, 2021; Mirchandani et al, 2020; Picht et al, 2012; Sollmann et al, 2017). Conversely, there is only limited data relating the temporal precision of CSV to the actual motor performance (Machetanz, Gallotti, et al, 2021; Machetanz et al, 2021).…”