Neural network alterations underlie cognitive deficits in brain tumor patients

Derks, Jolanda; Reijneveld, J.C.; Douw, Linda

doi:10.1097/cco.0000000000000126

Cited by 58 publications

(51 citation statements)

References 47 publications

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“…This slow‐wave oscillatory activity has been observed both within and between brain regions (Bajo et al, ; Dunkley et al, ; Hier et al, ). Furthermore, our findings of increased FC strength scores in PBT children are consistent with previous resting‐state research conducted in adult brain tumor survivors showing increased low frequency FC (Bartolomei et al, , ; Bosma et al, ; Derks, Reijneveld, & Douw, ). We have previously shown that PBT survivors display greater resting‐state theta power compared with healthy children (Dockstader et al, ).…”

Section: Discussionsupporting

confidence: 91%

Disrupted network connectivity in pediatric brain tumor survivors is a signature of injury

Gauvreau

Lefebvre

Bells

et al. 2019

J of Comparative Neurology

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Cognition is compromised in pediatric brain tumor survivors but the neurophysiological basis of this compromise remains unclear. We hypothesized that reduced neural synchronization across brain networks is involved. To test this, we evaluated group differences using a retrospective cohort comparison design between 24 pediatric brain tumor survivors [11.81 ± 3.27)] and 24 age matched healthy children [12.04 ± 3.28)] in functional connectivity within a cerebellar network to examine local effects of the tumor, a whole brain network to examine diffuse effects of treatment (i.e., chemotherapy and radiation), and across multiple intrinsic connectivity networks. Neural activity was recorded during magnetoencephalography scanning while participants were at rest and functional connectivity within networks was measured using the phase lag index. We corroborated our findings using a computational model representing the local tumor effects on neural synchrony. Compared to healthy children, pediatric brain tumor survivors show increased functional connectivity for theta and beta frequency bands within the cerebellar network and increased functional connectivity for the theta band within the whole brain network that again localized to the cerebellum. Computational modeling showed that increased synchrony in the theta bad is observed following local clustering as well as sparse interarea brain connectivity. We also observed increased functional connectivity for the alpha frequency band in the ventral attention network and decreased functional connectivity within the gamma frequency band in the motor network within paedatric brain tumor survivors versus healthy children. Notably, increased gamma functional connectivity within the motor network predicted decreased reaction time on behavioral tasks in pediatric brain tumor survivors. Disrupted network synchrony may be a signature of neurological injury and disease.

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Section: Discussionsupporting

confidence: 91%

Disrupted network connectivity in pediatric brain tumor survivors is a signature of injury

Gauvreau

Lefebvre

Bells

et al. 2019

J of Comparative Neurology

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“…In particular, four cognitive domains were examined that have been identified by previous studies to be affected by brain tumors: sustained attention, working memory, information processing speed, and executive functioning (Derks et al, 2014). One glioma patient was not tested because of lack of time, and one meningioma patient did not complete the sustained attention task.…”

Section: Methodsmentioning

confidence: 99%

Modeling Brain Dynamics in Brain Tumor Patients Using the Virtual Brain

Aerts

Schirner

Jeurissen

et al. 2018

eNeuro

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Presurgical planning for brain tumor resection aims at delineating eloquent tissue in the vicinity of the lesion to spare during surgery. To this end, noninvasive neuroimaging techniques such as functional MRI and diffusion-weighted imaging fiber tracking are currently employed. However, taking into account this information is often still insufficient, as the complex nonlinear dynamics of the brain impede straightforward prediction of functional outcome after surgical intervention. Large-scale brain network modeling carries the potential to bridge this gap by integrating neuroimaging data with biophysically based models to predict collective brain dynamics. As a first step in this direction, an appropriate computational model has to be selected, after which suitable model parameter values have to be determined. To this end, we simulated large-scale brain dynamics in 25 human brain tumor patients and 11 human control participants using The Virtual Brain, an open-source neuroinformatics platform. Local and global model parameters of the Reduced Wong–Wang model were individually optimized and compared between brain tumor patients and control subjects. In addition, the relationship between model parameters and structural network topology and cognitive performance was assessed. Results showed (1) significantly improved prediction accuracy of individual functional connectivity when using individually optimized model parameters; (2) local model parameters that can differentiate between regions directly affected by a tumor, regions distant from a tumor, and regions in a healthy brain; and (3) interesting associations between individually optimized model parameters and structural network topology and cognitive performance.

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“…The recruitment of homologous language-related areas in the contralesional cerebral hemisphere has been extensively verified in stroke and glioma patients (Desmurget et al, 2007;Duffau 2014;Thiel et al, 2005;Winhuisen et al, 2005;Yang et al, 2016). The second interpretation is to view the increased RSFC between network regions (i.e., hyperconnectivity) as a fundamental response to neurological disruption in patients with focal lesions or neurodegenerative/psychiatric diseases (Derks et al, 2014;Hillary & Grafman, 2017;Hillary et al, 2015). For example, SFG and MFG in the dominant hemisphere are charged with higher-order cognitive control, whereas dominant AG and IPL primarily undertake the role of linguistic comprehension (Fedorenko & Thompson-Schill, 2014;Wu et al, 2015).…”

Section: Alteration Of Cerebro-cerebellar Functional Connectivitymentioning

confidence: 98%

“…However, the neural mechanisms underlying cognitive impairments in glioma patients are largely unclear (Derks et al, 2017;Derks, Reijneveld, & Douw, 2014). However, the neural mechanisms underlying cognitive impairments in glioma patients are largely unclear (Derks et al, 2017;Derks, Reijneveld, & Douw, 2014).…”

Section: Introductionmentioning

confidence: 99%

Reorganization of cerebro‐cerebellar circuit in patients with left hemispheric gliomas involving language network: A combined structural and resting‐state functional MRI study

Zhang

Xia

Qiu

et al. 2018

Human Brain Mapping

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The role of cerebellum and cerebro-cerebellar system in neural plasticity induced by cerebral gliomas involving language network has long been ignored. Moreover, whether or not the process of reorganization is different in glioma patients with different growth kinetics remains largely unknown. To address this issue, we utilized preoperative structural and resting-state functional MRI data of 78 patients with left cerebral gliomas involving language network areas, including 46 patients with low-grade glioma (LGG, WHO grade II), 32 with high-grade glioma (HGG, WHO grade III/IV), and 44 healthy controls. Spontaneous brain activity, resting-state functional connectivity and gray matter volume alterations of the cerebellum were examined. We found that both LGG and HGG patients exhibited bidirectional alteration of brain activity in language-related cerebellar areas. Brain activity in areas with increased alteration was significantly correlated with the language and MMSE scores. Structurally, LGG patients exhibited greater gray matter volume in regions with increased brain activity, suggesting a structure-function coupled alteration in cerebellum. Furthermore, we observed that cerebellar regions with decreased brain activity exhibited increased functional connectivity with contralesional cerebro-cerebellar system in LGG patients. Together, our findings provide empirical evidence for a vital role of cerebellum and cerebro-cerebellar circuit in neural plasticity following lesional damage to cerebral language network. Moreover, we highlight the possible different reorganizational mechanisms of brain functional connectivity underlying different levels of behavioral impairments in LGG and HGG patients.

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Neural network alterations underlie cognitive deficits in brain tumor patients

Abstract: Cognitive deficits in brain tumor patients are reflected in whole-brain network disturbances. Possible future clinical use of these findings mostly concerns prognostics and tailoring treatment strategies.

Cited by 58 publications

References 47 publications

Disrupted network connectivity in pediatric brain tumor survivors is a signature of injury

Disrupted network connectivity in pediatric brain tumor survivors is a signature of injury

Modeling Brain Dynamics in Brain Tumor Patients Using the Virtual Brain

Reorganization of cerebro‐cerebellar circuit in patients with left hemispheric gliomas involving language network: A combined structural and resting‐state functional MRI study

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