Synchronized brain activity and neurocognitive function in patients with low-grade glioma: a magnetoencephalography study

Abstract

We investigated the mechanisms underlying neurocognitive dysfunction in patients with low-grade glioma (LGG) by relating functional connectivity revealed by magnetoencephalography to neurocognitive function. We administered a battery of standardized neurocognitive tests measuring six neurocognitive domains to a group of 17 LGG patients and 17 healthy controls, matched for age, sex, and educational level. Magnetoencephalography recordings were conducted during an eyes-closed "resting state," and synchronization likelihood (a measure of statistical correlation between signals) was computed from the delta to gamma frequency bands to assess functional connectivity between different brain areas. We found that, compared with healthy controls, LGG patients performed more poorly in psychomotor function, attention, information processing, and working memory. LGG patients also had significantly higher long-distance synchronization scores in the delta, theta, and lower gamma frequency bands than did controls. In contrast, patients displayed a decline in synchronization likelihood in the lower alpha frequency band. Within the delta, theta, and lower and upper gamma bands, increasing short- and long-distance connectivity was associated with poorer neurocognitive functioning. In summary, LGG patients showed a complex overall pattern of differences in functional resting-state connectivity compared with healthy controls. The significant correlations between neurocognitive performance and functional connectivity in various frequencies and across multiple brain areas suggest that the observed neurocognitive deficits in these patients can possibly be attributed to differences in functional connectivity due to tumor and/or treatment.

Fig. 1

Flow diagram of the relationship between tumor-related factors, higher neurocognitive function, and functional connectivity in patients with low-grade glioma. Abbreviations: fMRI, functional MRI; EEG, electroencephalography; MEG, magnetoencephalography.

Fig. 2

Distribution of magnetoencephalography (MEG) regions and illustration of short-distance (dashed arrow) and long-distance (solid arrow) connections.

Fig. 3

Patients’ z-scores on the six neurocognitive domains on total neurocognitive functioning. Abbreviations: PF, psychomotor functioning; A, attention; IPS, information processing speed; VM, verbal memory; WM, working memory; EF, executive functioning. Performance is relative to that of age-, sex-, and education-matched healthy controls (represented by the “0” line). A higher score (i.e., approaching 0) indicates better performance. *p ⩽ 0.05, **p ⩽ 0.01.

Fig. 4

Significant differences in long-distance connectivity between low-grade glioma patients and healthy controls in the different frequency bands. Gray arrows indicate significantly higher synchronization in the patient group. Black arrows indicate significantly lower synchronization in the patient group. Abbreviations: LF, left frontal; RF, right frontal; LT, left temporal; LC, left central; RC, right central; RT, right temporal; LP, left parietal; RP, right parietal; LO, left occipital; RO, right occipital.

Fig. 5

Significant differences in the long-distance connectivity between synchronization likelihood scores in low-grade glioma patients and neurocognitive function in the different frequency bands. Black arrows and areas indicate higher synchronization associated with worsening in higher neurocognitive functioning. Gray arrows and areas indicate higher synchronization associated with improving higher neurocognitive functioning. Abbreviations: LF, left frontal; RF, right frontal; LT, left temporal; LC, left central; RC, right central; RT, right temporal; LP, left parietal; RP, right parietal; LO, left occipital; RO, right occipital.