Brain tumors disrupt the resting-state connectome

Hadjiabadi, Darian; Pung, Leland; Zhang, Jiangyang; Ward, B. Douglas; Lim, Wantae; Kalavar, Meghana; Thakor, Nitish V.; Biswal, Bharat B.; Pathak, Arvind P.

doi:10.1016/j.nicl.2018.01.026

Cited by 37 publications

(30 citation statements)

References 58 publications

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“…In regard to resting-state fMRI, our results suggest that both neuronal desynchronization and neurovascular disruption could contribute to apparent changes in fMRI-based measures of “functional connectivity” related to tumor progression ( Dierker et al, 2017 ; Hadjiabadi et al, 2018 ). Nevertheless, these results do suggest a firm physiological basis for studies that have noted the ability of resting state fMRI data to delineate glioma tumor boundaries ( Agarwal et al, 2016 ; Bowden et al, 2018 ; Chow et al, 2016 ).…”

Section: Discussionmentioning

confidence: 92%

Glioma-Induced Alterations in Neuronal Activity and Neurovascular Coupling during Disease Progression

et al. 2020

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SUMMARY Diffusely infiltrating gliomas are known to cause alterations in cortical function, vascular disruption, and seizures. These neurological complications present major clinical challenges, yet their underlying mechanisms and causal relationships to disease progression are poorly characterized. Here, we follow glioma progression in awake Thy1-GCaMP6f mice using in vivo wide-field optical mapping to monitor alterations in both neuronal activity and functional hemodynamics. The bilateral synchrony of spontaneous neuronal activity gradually decreases in glioma-infiltrated cortical regions, while neurovascular coupling becomes progressively disrupted compared to uninvolved cortex. Over time, mice develop diverse patterns of high amplitude discharges and eventually generalized seizures that appear to originate at the tumors’ infiltrative margins. Interictal and seizure events exhibit positive neurovascular coupling in uninfiltrated cortex; however, glioma-infiltrated regions exhibit disrupted hemodynamic responses driving seizure-evoked hypoxia. These results reveal a landscape of complex physiological interactions occurring during glioma progression and present new opportunities for exploring novel biomarkers and therapeutic targets.

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Section: Discussionmentioning

confidence: 92%

Glioma-Induced Alterations in Neuronal Activity and Neurovascular Coupling during Disease Progression

et al. 2020

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“…It is also in line with the concept of GBM being a disease that involves the entire brain, which is best exemplified by its highly invasive growth capacity with single tumour cells that invade the most distant brain regions 8 , 24 . Indeed, a more extensive impact on neurologic function and network connectivity than merely explained by the macroscopic mass lesion has been documented for interhemispheric connections 18 , 25 , 26 . Here, we advance this concept of GBM as a whole brain disease by highlighting the fact that tumour-related network alterations may be spatially widely distributed as long as they are functionally close.…”

Section: Discussionmentioning

confidence: 99%

Distributed changes of the functional connectome in patients with glioblastoma

Nenning

Furtner

Kiesel

et al. 2020

Sci Rep

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Glioblastoma might have widespread effects on the neural organization and cognitive function, and even focal lesions may be associated with distributed functional alterations. However, functional changes do not necessarily follow obvious anatomical patterns and the current understanding of this interrelation is limited. In this study, we used resting-state functional magnetic resonance imaging to evaluate changes in global functional connectivity patterns in 15 patients with glioblastoma. For six patients we followed longitudinal trajectories of their functional connectome and structural tumour evolution using bi-monthly follow-up scans throughout treatment and disease progression. In all patients, unilateral tumour lesions were associated with inter-hemispherically symmetric network alterations, and functional proximity of tumour location was stronger linked to distributed network deterioration than anatomical distance. In the longitudinal subcohort of six patients, we observed patterns of network alterations with initial transient deterioration followed by recovery at first follow-up, and local network deterioration to precede structural tumour recurrence by two months. In summary, the impact of focal glioblastoma lesions on the functional connectome is global and linked to functional proximity rather than anatomical distance to tumour regions. Our findings further suggest a relevance for functional network trajectories as a possible means supporting early detection of tumour recurrence.

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“…In regards to resting-state fMRI, our results suggest that both neuronal desynchronization and neurovascular disruption could contribute to apparent changes in fMRI-based measures of 'functional connectivity' related to tumor progression (Hadjiabadi et al, 2018) (Dierker et al, 2017). Nevertheless, these results do suggest a firm physiological basis for studies which have noted the ability of resting state fMRI data to delineate glioma tumor boundaries (Bowden et al, 2018) (Chow et al, 2016) (Agarwal et al, 2016).…”

Section: Progressive Disruption Of Neurovascular Couplingmentioning

confidence: 66%

Glioma-induced alterations in neuronal activity and neurovascular coupling during disease progression

Montgomery

Kim

Dovas

et al. 2019

Preprint

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AbstractDiffusely infiltrating gliomas are known to cause alterations in cortical function, vascular disruption and seizures. These neurological complications present major clinical challenges, yet their underlying mechanisms and causal relationships to disease progression are poorly characterized. Here, we followed glioma progression in awake Thy1-GCaMP6f mice using in-vivo wide-field optical mapping to monitor alterations in both neuronal activity and functional hemodynamics. The bilateral synchrony of spontaneous neuronal activity in glioma-infiltrated cortex gradually decreased, while neurovascular coupling was also progressively disrupted compared to uninvolved cortex. Over time, mice developed diverse patterns of high amplitude discharges and eventually generalized seizures that begin at the infiltrative margin of the tumors. Interictal and seizure events exhibited positive neurovascular coupling in uninfiltrated cortex, however glioma-infiltrated regions exhibited inverted hemodynamic responses driving seizure-evoked hypoxia. These results reveal a landscape of complex physiological interactions occurring during glioma progression and present new opportunities for exploring new biomarkers and therapeutic targets.Highlights-Glioma disrupts neural synchrony between bilateral cortical regions.-WFOM reveals frequent interictal discharges and seizures during glioma progression.-Tumor development is accompanied by local changes in neurovascular coupling.-Altered neurovascular coupling drives hypoperfusion of the tumor during seizures.

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Brain tumors disrupt the resting-state connectome

Cited by 37 publications

References 58 publications

Glioma-Induced Alterations in Neuronal Activity and Neurovascular Coupling during Disease Progression

Glioma-Induced Alterations in Neuronal Activity and Neurovascular Coupling during Disease Progression

Distributed changes of the functional connectome in patients with glioblastoma

Glioma-induced alterations in neuronal activity and neurovascular coupling during disease progression

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