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Showing content from https://pubmed.ncbi.nlm.nih.gov/28050345/ below:

Functional MRI vs. navigated TMS to optimize M1 seed volume delineation for DTI tractography. A prospective study in patients with brain tumours adjacent to the corticospinal tract

Comparative Study

. 2016 Nov 23:13:297-309. doi: 10.1016/j.nicl.2016.11.022. eCollection 2017. Functional MRI vs. navigated TMS to optimize M1 seed volume delineation for DTI tractography. A prospective study in patients with brain tumours adjacent to the corticospinal tract Irada Tursunova¹, Volker Neuschmelting¹, Charlotte Nettekoven¹, Ana-Maria Oros-Peusquens², Gabriele Stoffels², Andrea Maria Faymonville¹, Shah N Jon³, Karl Josef Langen⁴, Hannah Lockau⁵, Roland Goldbrunner¹, Christian Grefkes⁶

Affiliations

¹ University of Cologne, Center of Neurosurgery, 50924 Cologne, Germany.
² Institute of Neuroscience and Medicine, Research Centre Jülich, 52425 Jülich, Germany.
³ Institute of Neuroscience and Medicine, Research Centre Jülich, 52425 Jülich, Germany; RWTH Aachen University, University Clinic Aachen, Departments of Nuclear Medicine and Neurology, 52074 Aachen, Germany; Department of Electrical and Computer Systems Engineering, Monash University, Melbourne, Victoria, Australia; Monash Institute of Medical Engineering, Monash University, Melbourne, Victoria, Australia; Monash Biomedical Imaging, School of Psychological Sciences, Monash University, Melbourne, Victoria, Australia.
⁴ Institute of Neuroscience and Medicine, Research Centre Jülich, 52425 Jülich, Germany; RWTH Aachen University, University Clinic Aachen, Departments of Nuclear Medicine and Neurology, 52074 Aachen, Germany.
⁵ University of Cologne, Department of Radiology, 50937 Cologne, Germany.
⁶ Institute of Neuroscience and Medicine, Research Centre Jülich, 52425 Jülich, Germany; University of Cologne, Department of Neurology, 50924 Cologne, Germany.

PMID: 28050345
PMCID: PMC5192048
DOI: 10.1016/j.nicl.2016.11.022

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Comparative Study

Functional MRI vs. navigated TMS to optimize M1 seed volume delineation for DTI tractography. A prospective study in patients with brain tumours adjacent to the corticospinal tract

Carolin Weiss Lucas et al. Neuroimage Clin. 2016.

. 2016 Nov 23:13:297-309. doi: 10.1016/j.nicl.2016.11.022. eCollection 2017. Authors Carolin Weiss Lucas¹, Irada Tursunova¹, Volker Neuschmelting¹, Charlotte Nettekoven¹, Ana-Maria Oros-Peusquens², Gabriele Stoffels², Andrea Maria Faymonville¹, Shah N Jon³, Karl Josef Langen⁴, Hannah Lockau⁵, Roland Goldbrunner¹, Christian Grefkes⁶ Affiliations

¹ University of Cologne, Center of Neurosurgery, 50924 Cologne, Germany.
² Institute of Neuroscience and Medicine, Research Centre Jülich, 52425 Jülich, Germany.
³ Institute of Neuroscience and Medicine, Research Centre Jülich, 52425 Jülich, Germany; RWTH Aachen University, University Clinic Aachen, Departments of Nuclear Medicine and Neurology, 52074 Aachen, Germany; Department of Electrical and Computer Systems Engineering, Monash University, Melbourne, Victoria, Australia; Monash Institute of Medical Engineering, Monash University, Melbourne, Victoria, Australia; Monash Biomedical Imaging, School of Psychological Sciences, Monash University, Melbourne, Victoria, Australia.
⁴ Institute of Neuroscience and Medicine, Research Centre Jülich, 52425 Jülich, Germany; RWTH Aachen University, University Clinic Aachen, Departments of Nuclear Medicine and Neurology, 52074 Aachen, Germany.
⁵ University of Cologne, Department of Radiology, 50937 Cologne, Germany.
⁶ Institute of Neuroscience and Medicine, Research Centre Jülich, 52425 Jülich, Germany; University of Cologne, Department of Neurology, 50924 Cologne, Germany.

PMID: 28050345
PMCID: PMC5192048
DOI: 10.1016/j.nicl.2016.11.022

Item in Clipboard

Abstract

Background: DTI-based tractography is an increasingly important tool for planning brain surgery in patients suffering from brain tumours. However, there is an ongoing debate which tracking approaches yield the most valid results. Especially the use of functional localizer data such as navigated transcranial magnetic stimulation (nTMS) or functional magnetic resonance imaging (fMRI) seem to improve fibre tracking data in conditions where anatomical landmarks are less informative due to tumour-induced distortions of the gyral anatomy. We here compared which of the two localizer techniques yields more plausible results with respect to mapping different functional portions of the corticospinal tract (CST) in brain tumour patients.

Methods: The CSTs of 18 patients with intracranial tumours in the vicinity of the primary motor area (M1) were investigated by means of deterministic DTI. The core zone of the tumour-adjacent hand, foot and/or tongue M1 representation served as cortical regions of interest (ROIs). M1 core zones were defined by both the nTMS hot-spots and the fMRI local activation maxima. In addition, for all patients, a subcortical ROI at the level of the inferior anterior pons was implemented into the tracking algorithm in order to improve the anatomical specificity of CST reconstructions. As intra-individual control, we additionally tracked the CST of the hand motor region of the unaffected, i.e., non-lesional hemisphere, again comparing fMRI and nTMS M1 seeds. The plausibility of the fMRI-ROI- vs. nTMS-ROI-based fibre trajectories was assessed by a-priori defined anatomical criteria. Moreover, the anatomical relationship of different fibre courses was compared regarding their distribution in the anterior-posterior direction as well as their location within the posterior limb of the internal capsule (PLIC).

Results: Overall, higher plausibility rates were observed for the use of nTMS- as compared to fMRI-defined cortical ROIs (p < 0.05) in tumour vicinity. On the non-lesional hemisphere, however, equally good plausibility rates (100%) were observed for both localizer techniques. fMRI-originated fibres generally followed a more posterior course relative to the nTMS-based tracts (p < 0.01) in both the lesional and non-lesional hemisphere.

Conclusion: NTMS achieved better tracking results than fMRI in conditions when the cortical tract origin (M1) was located in close vicinity to a brain tumour, probably influencing neurovascular coupling. Hence, especially in situations with altered BOLD signal physiology, nTMS seems to be the method of choice in order to identify seed regions for CST mapping in patients.

Keywords: APB, Abductor pollicis brevis muscle; BOLD, Blood-oxygenation-level dependent; CST; CST, Corticospinal tract; DCS, Direct cortical stimulation; DTI, Diffusion tensor imaging; Deterministic; EF, Electric field; EMG, Electromyography; FA(T), Fractional anisotropy (threshold); FACT, Fibre assignment by continuous tracking; FOV, Field-of-view; FWE, Family-wise error; KPS, Karnofsky performance scale; LT, Lateral tongue muscle, anterior third; M1, Primary motor cortex; MEP, Motor-evoked potential; MFL, Minimal fibre length; MPRAGE, Magnetization prepared rapid acquisition gradient echo (T1 MR seq.); OR, Odd's ratio; PLIC, Posterior limb of the internal capsule; PM, Plantar muscle; Pyramidal tract; RMT, Resting motor threshold; ROI; ROI, Region-of-interest; SD, Standard deviation; SE, Standard error; Somatotopic; X-sq, X-squared (Pearson's chi-square test); dMRI, Diffusion magnetic resonance imaging (i.e., diffusion-weighted imaging, DWI); fMRI; fMRI, Functional magnetic resonance imaging; nTMS; nTMS, Neuronavigated transcranial magnetic stimulation; pxsq, p-value according to Pearson's chi-square test.

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Figures
Fig. S1

Hand-M1-derived CST. A pair of…

Fig. S1

Hand-M1-derived CST. A pair of somatotopic CST fibres derived from the hand representation…

Fig. S1

Hand-M1-derived CST. A pair of somatotopic CST fibres derived from the hand representation as delineated based on either fMRI (yellow) or nTMS (red) are shown. The nTMS-derived fibre follows a plausible pathway whereas the fMRI-derived tract was rated non-plausible by the two raters. This case exemplifies the huge dependency of the tractography results on the accuracy of the (sub-)cortical seeding ROI.

Fig. S2

Tongue-M1-derived CST. Somatotopic CST fibres…

Fig. S2

Tongue-M1-derived CST. Somatotopic CST fibres originating from the fMRI (yellow) vs. nTMS (red)…

Fig. S2

Tongue-M1-derived CST. Somatotopic CST fibres originating from the fMRI (yellow) vs. nTMS (red) tongue representation illustrating the rare condition of non-plausible nTMS-based fibre course in a case where the use of fMRI to delineate the origin ROI led to a plausible fibre reconstruction (with the same second, pontine ROI). Here, also the FAT had to be lowered considerably (0.04 vs. 0.13) using the nTMS as compared to the fMRI approach to allow reconstruction of at least one fibre connecting the cortical ROI to the pontine ROI. In general but particularly when applying such low FAT values for fibre reconstruction in the tumour surrounding tissue, tractography results have to be interpreted with caution since crossing fibres and diffusion artefacts can lead to non-plausible tracts.

Fig. 1

Cortical regions of interest representing…

Fig. 1

Cortical regions of interest representing the M1 core area. For each functional localizer…

Fig. 1

Cortical regions of interest representing the M1 core area. For each functional localizer method, i.e., nTMS, fMRI and DCS, the core area (hot-spot/local activation maxima) was separately determined, integrated into the neuronavigation software and enlarged to a spherical volume of 0.9 cm³ (± 0.1) (here: hand representation). Here, a patient with postcentral glioma (contrast-enhancing tumour volume outlined in dark blue) with strong perifocal oedema (outlined in light blue) is shown. The hot-spot of the M1 hand representation depicted by nTMS prior to surgery (red) was very close to the DCS hot-spot (orange) whereas the fMRI local activation maximum (yellow) was located slightly posteriorly and deeper within the white matter.

Fig. 2

Placement of the cubic subcortical…

Fig. 2

Placement of the cubic subcortical ROI in the anterior inferior pontine region. According…

Fig. 2

Placement of the cubic subcortical ROI in the anterior inferior pontine region. According to our previous study (Weiss et al., 2015) a second subcortical ROI box (in addition to the functional cortical ROI) was set in the anterior inferior pontine region in order to apply a deterministic multiple-ROI tractography approach (Mori et al., 2002). To control for the field-of-view and artefacts in the DTI data set, the ROI placement was based on both anatomical T1 (left) and DTI series (B0 sequence; right).

Fig. 3

Functional-localizer-derived somatotopic DTI-tractography. A pair…

Fig. 3

Functional-localizer-derived somatotopic DTI-tractography. A pair of somatotopic corticospinal tracts originating from the cortical…

Fig. 3

Functional-localizer-derived somatotopic DTI-tractography. A pair of somatotopic corticospinal tracts originating from the cortical functional core representation of the as defined by either fMRI (yellow) or nTMS (red), both rated plausible tracts. Examples for mixed plausible/non-plausible tractography results with somatotopic hand/face affiliation are provided in the Supplementary material (Supplementary Fig. S1, Fig. S2). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Functional-localizer-derived somatotopic DTI-tractography. A pair of somatotopic corticospinal tracts originating from the cortical functional core representation of the as defined by either fMRI (yellow) or nTMS (red), both rated plausible tracts. Examples for mixed plausible/non-plausible tractography results with somatotopic hand/face affiliation are provided in the Supplementary material (Supplementary Figs. S1 and S2).

Fig. 4

Segmentation of the PLIC: The…

Fig. 4

Segmentation of the PLIC: The PLIC was segmented into three parts of equal…

Fig. 4

Segmentation of the PLIC: The PLIC was segmented into three parts of equal length: the most rostral/central (c) segment of which included the genu; the other two parts were treated as the middle (m) and posterior (p) segment. Each fibre tract (yellow/red) was assigned to one of the segments, according to the location of its major part in the axial cross-sectional view on the level of the interventricular foramen of Monro. In this example, showing somatotopic fibres originating from the cortical M1 hot-spot/local activation maximum of the hand, both fMRI- (yellow) and nTMS- (red) derived fibre tracts were located in the posterior section of the PLIC.

Fig. 5

Plausibility rates of somatotopic CST…

Fig. 5

Plausibility rates of somatotopic CST courses. The bar plot displays the plausibility rates…

Fig. 5

Plausibility rates of somatotopic CST courses. The bar plot displays the plausibility rates (y: count of plausible tracts in % of total) and absolute numbers regarding the course of the somatotopic CST. The distinct somatotopic core ROIs within the primary motor cortex (columns) served as origins for the tracking algorithm and were determined by either nTMS (darker grey) or fMRI (light grey).

Fig. 6

Course of somatotopic CST fibres…

Fig. 6

Course of somatotopic CST fibres within the PLIC. The bar plots display the…

Fig. 6

Course of somatotopic CST fibres within the PLIC. The bar plots display the distribution of the somatotopic CST fibres, originating from the cortical nTMS- (grey), fMRT- (light grey) and DCS- (dark grey) ROIs, within the PLIC. For this analysis, the PLIC was segmented into a central section including the genu (c), a middle (m) and a posterior section (p), according to Fig. 4. The figure includes the percentages of fibres in each segment per total of the respective functional localizer technique (Y-axis) as well as the respective count data (numbers above each bar).