Recovery of functional connectivity of the sensorimotor network after surgery for diffuse low-grade gliomas involving the supplementary motor area.
01 Apr 2017-Journal of Neurosurgery (American Association of Neurological Surgeons)-Vol. 126, Iss: 4, pp 1181-1190
TL;DR: The results confirm the findings reported in the existing literature on the plasticity of the SMA, showing large-scale modifications of the sensorimotor network, at both inter- and intrahemispheric levels and suggest that interhemispherical connectivity might be a correlate of SMA syndrome recovery.
Abstract: OBJECTIVE The supplementary motor area (SMA) syndrome is a well-studied lesional model of brain plasticity involving the sensorimotor network. Patients with diffuse low-grade gliomas in the SMA may exhibit this syndrome after resective surgery. They experience a temporary loss of motor function, which completely resolves within 3 months. The authors used functional MRI (fMRI) resting state analysis of the sensorimotor network to investigate large-scale brain plasticity between the immediate postoperative period and 3 months' follow-up. METHODS Resting state fMRI was performed preoperatively, during the immediate postoperative period, and 3 months postoperatively in 6 patients with diffuse low-grade gliomas who underwent partial surgical excision of the SMA. Correlation analysis within the sensorimotor network was carried out on those 3 time points to study modifications of its functional connectivity. RESULTS The results showed a large-scale reorganization of the sensorimotor network. Interhemispheric connectivity was decreased in the postoperative period, and increased again during the recovery process. Connectivity between the lesion side motor area and the contralateral SMA rose to higher values than in the preoperative period. Intrahemispheric connectivity was decreased during the immediate postoperative period and had returned to preoperative values at 3 months after surgery. CONCLUSIONS These results confirm the findings reported in the existing literature on the plasticity of the SMA, showing large-scale modifications of the sensorimotor network, at both inter- and intrahemispheric levels. They suggest that interhemispheric connectivity might be a correlate of SMA syndrome recovery.
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TL;DR: This review examines the structural connectivity of a recently-identified fiber pathway, the frontal aslant tract (FAT), and suggests that the FAT plays a domain general role in the planning, timing, and coordination of sequential motor movements through the resolution of competition among potential motor plans.
143 citations
TL;DR: It is found that a greater extent of resection could significantly increase the OS of patients with low-grade gliomas.
Abstract: Surgical resection is necessary to conduct a pathological biopsy and to achieve a reduction of intracranial pressure in low-grade gliomas patients. This study aimed to determine whether a greater extent of resection would increase the overall 5-year and 10-year survival of patients with low-grade gliomas. The studies addressing relationship between the extent of resection and the prognosis of low-grade gliomas updated until March 2017 were systematically searched in two databases (Pubmed and EMBASE). The relationships among categorical variables were analyzed using an odds ratio (OR) and a95% confidence interval (CI). Significance was established using CIs at a level of 95% or P < 0.05. Funnel plot was used to detect the publication bias. Twenty articles (a total of 2128 patients) were identified. The meta-analysis showed that the 5-year (Odds ratio (OR), 3.90;95% Confidence Interval (CI), 2.79~5.45; P < 0.01; Z = 7.95) and 10-year OS (OR, 7.91; 95%CI, 5.12~12.22; P < 0.01; Z = 9.33) associated with gross total resection (GTR) were higher than those associated with subtotal resection (STR). Similarly, as compared with biopsy(BX), the 5-year and 10-year OS were higher after either GTR (5-year: OR, 5.43; 95%CI, 3.57~8.26; P < 0.01; Z = Z = 7.9; 10-year: OR, 10.17; 95%CI, 4.02~25.71; P < 0.00001; Z = 4.9) or STR (5-year: OR, 2.59; 95%CI, 1.81~ − 3.71; P < 0.00001; Z = 5.19; 10-year: OR, 2.21; 95%CI, 1.164.25; P = 0.02; Z = 2.39). Our research found that a greater extent of resection could significantly increase the OS of patients with low-grade gliomas.
71 citations
Cites background from "Recovery of functional connectivity..."
...Surgical resection of low-grade gliomas may lead to dysfunction and impairment of patients’ quality of life (QOL) [31]....
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...The midline of the studies indicates a slight publication bias of studies showing benefit with GTR over STR. (PDF 12 kb) Abbreviations BX: Biopsy; Ch: Chemotherapy not otherwise specified; CI: Confidence interval; GTR: Gross total resection; NCI: National Cancer Institute; NS: Not stated; OR: Odds ratio; OS: Overall survival; PFS: Progression-free survival; QOL: Quality of life; RCT: Randomized and controlled trial; RT: Radiation therapy; STR: Subtotal resection Acknowledgements We thank Dr. Ping Zhang for her help in reviewing the manuscript....
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TL;DR: More efficient plasticity mechanisms are facilitated by cortical tumors with sharp borders, are associated with an increase of EOR at reoperation and with earlier functional recovery in diffuse glioma patients.
Abstract: BACKGROUND In diffuse glioma, a multistage approach with iterative tailored surgical resections can be considered. OBJECTIVE To compare results of iterative intrasurgical brain mappings to investigate the potential and limitation of neuroplasticity at the individual stage, and to highlight to what extent it can influence the therapeutic strategy. METHODS Glioma patients who underwent 2 consecutive awake surgeries with cortical and subcortical stimulation were classified into group 1 (n = 23) if cortical mappings exhibited high level of plasticity (displacement of ≥2 sites) or into group 2 (n = 19) with low level of plasticity. RESULTS Clinical characteristics did not differ significantly between both groups. The borders of the tumors were mostly sharp in group 1 (82.6%) and rather indistinct in group 2 (84.2%), (P = .00001). Tumor remnants were more often cortical (± subcortical) in group 1 (39.1%) and more often purely subcortical in group 2 (68.4%; P = .009). In group 1, the time needed to recover independence was significantly shorter at reoperation (37.6 h vs 78.3 h after the first surgery, P = .00003) while this difference was not significant in group 2. The iterative extents of resection (EOR) remain comparable in group 1 (94% vs 92%, P = .40) but were significantly smaller in group 2 at reoperation (94% vs 88%, P = .05). CONCLUSION More efficient plasticity mechanisms are facilitated by cortical tumors with sharp borders, are associated with an increase of EOR at reoperation and with earlier functional recovery. Tumoral invasion of the white matter tracts represents the main limitation of neuroplasticity: this connectomal constraint limits EOR during second surgery.
71 citations
TL;DR: This review examines the structural connectivity of a recently-identified fiber pathway, the frontal aslant tract (FAT), and suggests that the FAT plays a domain general role in the planning, timing, and coordination of sequential motor movements through the resolution of competition among potential motor plans.
Abstract: In this review, we examine the structural connectivity of a recently-identified fiber pathway, the frontal aslant tract (FAT), and explore its function. We first review structural connectivity studies using tract-tracing methods in non-human primates, and diffusion-weighted imaging and electrotimulation in humans. These studies suggest a monosynaptic connection exists between the lateral inferior frontal gyrus and the pre-supplementary and supplementary motor areas of the medial superior frontal gyrus. This connection is termed the FAT. We then review research on the left FAT9s putative role in supporting speech and language function, with particular focus on speech initiation, stuttering, verbal fluency and language more broadly. Next, we review research on the right FAT9s putative role supporting executive function, namely inhibitory control and conflict monitoring. We summarize the extant body of empirical work by suggesting that the FAT plays a domain general role in the planning, timing, and coordination of sequential motor movements, and in the resolution of competition among possible cognitive and motor plans. However, we also propose some domain specialization across the hemispheres. On the left hemisphere, the circuit is proposed to be specialized for speech actions. On the right hemisphere, the circuit is proposed to be specialized for general action control of the organism, especially in the visuo-spatial domain. We close the review with a discussion of the clinical significance of the FAT, and suggestions for further research on the pathway.
67 citations
Cites background from "Recovery of functional connectivity..."
...…resolving within weeks to months (Bannur & Rajshekhar, 2000; Laplane et al., 1977; Potgieser et al., 2014), with days to recovery correlated with interhemispheric connectivity between the SMA and the primary motor cortex (Oda, Yamaguchi, Enomoto, Higuchi, & Morita, 2018; M. Vassal et al., 2017)....
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TL;DR: Noninvasive functional MRI techniques may offer the opportunity to perform a multimodal assessment in brain tumors, to be integrated with intraoperative mapping and clinical data for improving surgical management and oncological and functional outcome in patients affected by gliomas.
Abstract: Advanced neuroimaging techniques such as functional MRI (fMRI) and diffusion MR tractography have been increasingly used at every stage of the surgical management of brain gliomas, as a means to improve tumor resection while preserving brain functions. This review provides an overview of the last advancements in the field of functional MRI techniques, with a particular focus on their current clinical use and reliability in the preoperative and intraoperative setting, as well as their future perspectives for personalized multimodal management of patients with gliomas. fMRI and diffusion MR tractography give relevant insights on the anatomo-functional organization of eloquent cortical areas and subcortical connections near or inside a tumor. Task-based fMRI and diffusion tensor imaging (DTI) tractography have proven to be valid and highly sensitive tools for localizing the distinct eloquent cortical and subcortical areas before surgery in glioma patients; they also show good accuracy when compared with intraoperative stimulation mapping data. Resting-state fMRI functional connectivity as well as new advanced HARDI (high angular resolution diffusion imaging) tractography methods are improving and reshaping the role of functional MRI for surgery of gliomas, with potential benefit for personalized treatment strategies. Noninvasive functional MRI techniques may offer the opportunity to perform a multimodal assessment in brain tumors, to be integrated with intraoperative mapping and clinical data for improving surgical management and oncological and functional outcome in patients affected by gliomas.
58 citations
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33,268 citations
TL;DR: It is concluded that correlation of low frequency fluctuations, which may arise from fluctuations in blood oxygenation or flow, is a manifestation of functional connectivity of the brain.
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8,766 citations
Rutgers University1, New York University2, University of Oxford3, Harvard University4, Bangor University5, University of Copenhagen6, National Institutes of Health7, Oregon Health & Science University8, Yale University9, Nathan Kline Institute for Psychiatric Research10, Medical College of Wisconsin11, University of Oulu12, Radboud University Nijmegen13, National Yang-Ming University14, Cleveland Clinic15, Duke University16, Max Planck Society17, Emory University18, University of Queensland19, University of Michigan20, Kennedy Krieger Institute21, Washington University in St. Louis22, Technische Universität München23, Leiden University24, University of Texas at Dallas25, Charité26, University of Pittsburgh27, Southeast University28, Otto-von-Guericke University Magdeburg29, Massachusetts Institute of Technology30, University of Western Ontario31, Medical University of Vienna32, Beijing Normal University33
TL;DR: The 1000 Functional Connectomes Project (Fcon_1000) as discussed by the authors is a large-scale collection of functional connectome data from 1,414 volunteers collected independently at 35 international centers.
Abstract: Although it is being successfully implemented for exploration of the genome, discovery science has eluded the functional neuroimaging community. The core challenge remains the development of common paradigms for interrogating the myriad functional systems in the brain without the constraints of a priori hypotheses. Resting-state functional MRI (R-fMRI) constitutes a candidate approach capable of addressing this challenge. Imaging the brain during rest reveals large-amplitude spontaneous low-frequency (<0.1 Hz) fluctuations in the fMRI signal that are temporally correlated across functionally related areas. Referred to as functional connectivity, these correlations yield detailed maps of complex neural systems, collectively constituting an individual's "functional connectome." Reproducibility across datasets and individuals suggests the functional connectome has a common architecture, yet each individual's functional connectome exhibits unique features, with stable, meaningful interindividual differences in connectivity patterns and strengths. Comprehensive mapping of the functional connectome, and its subsequent exploitation to discern genetic influences and brain-behavior relationships, will require multicenter collaborative datasets. Here we initiate this endeavor by gathering R-fMRI data from 1,414 volunteers collected independently at 35 international centers. We demonstrate a universal architecture of positive and negative functional connections, as well as consistent loci of inter-individual variability. Age and sex emerged as significant determinants. These results demonstrate that independent R-fMRI datasets can be aggregated and shared. High-throughput R-fMRI can provide quantitative phenotypes for molecular genetic studies and biomarkers of developmental and pathological processes in the brain. To initiate discovery science of brain function, the 1000 Functional Connectomes Project dataset is freely accessible at www.nitrc.org/projects/fcon_1000/.
2,787 citations
TL;DR: In this article, the authors discuss the basic quantitative features of the observed BOLD-based signal changes, including the signal amplitude and its magnetic field dependence and dynamic effects such as a pronounced oscillatory pattern that is induced in the signal from primary visual cortex during photic stimulation experiments.
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TL;DR: The findings provide a solid foundation for continued examination of resting state fcMRI in typical and atypical populations, and short- and long-term measures of the consistency of global connectivity patterns were highly robust.
Abstract: Recent years have witnessed an upsurge in the usage of resting-state functional magnetic resonance imaging (fMRI) to examine functional connectivity (fcMRI), both in normal and pathological populations. Despite this increasing popularity, concerns about the psychologically unconstrained nature of the “resting-state” remain. Across studies, the patterns of functional connectivity detected are remarkably consistent. However, the test–retest reliability for measures of resting state fcMRI measures has not been determined. Here, we quantify the test–retest reliability, using resting scans from 26 participants at 3 different time points. Specifically, we assessed intersession (>5 months apart), intrasession ( nonsignificant), 2) correlation valence (positive > negative), and 3) network membership (default mode > task positive network). Short- and long-term measures of the consistency of global connectivity patterns were highly robust. Finally, hierarchical clustering solutions were highly reproducible, both across participants and sessions. Our findings provide a solid foundation for continued examination of resting state fcMRI in typical and atypical populations.
905 citations