Synchronization during an internally directed cognitive state in healthy aging and mild cognitive impairment: a MEG study

Abstract

Mild cognitive impairment (MCI) is a stage between healthy aging and dementia. It is known that in this condition the connectivity patterns are altered in the resting state and during cognitive tasks, where an extra effort seems to be necessary to overcome cognitive decline. We aimed to determine the functional connectivity pattern required to deal with an internally directed cognitive state (IDICS) in healthy aging and MCI. This task differs from the most commonly employed ones in neurophysiology, since inhibition from external stimuli is needed, allowing the study of this control mechanism. To this end, magnetoencephalographic (MEG) signals were acquired from 32 healthy individuals and 38 MCI patients, both in resting state and while performing a subtraction task of two levels of difficulty. Functional connectivity was assessed with phase locking value (PLV) in five frequency bands. Compared to controls, MCIs showed higher PLV values in delta, theta, and gamma bands and an opposite pattern in alpha, beta, and gamma bands in resting state. These changes were associated with poorer neuropsychological performance. During the task, this group exhibited a hypersynchronization in delta, theta, beta, and gamma bands, which was also related to a lower cognitive performance, suggesting an abnormal functioning in this group. Contrary to controls, MCIs presented a lack of synchronization in the alpha band which may denote an inhibition deficit. Additionally, the magnitude of connectivity changes rose with the task difficulty in controls but not in MCIs, in line with the compensation-related utilization of neural circuits hypothesis (CRUNCH) model.

Fig. 1

MEG sensor layout. Magnetometer positions in 2D and 3D, separated into frontal, parietal, occipital, and left and right temporal regions

Fig. 2

Statistical differences in connectivity between resting and 3-substraction task for controls and MCIs. Significantly altered links (p < 0.005) are shown for every frequency band. A line between two nodes represents a link that has been significantly altered and is either decreased (resting > task) or increased (task > testing) in the 3-substraction task. For clarity in visualization, only a selection of links was displayed: firstly, in order to reduce loose links, nodes participating with a single significant link were discarded, and secondly, a maximum of 150 links was plotted (if more links were statistically significant, 150 links with the lowest p value were chosen)

Fig. 3

Number of significantly altered links when comparing resting and task for different groups and frequency bands. The first row shows differences between 1-substraction task (gray) and resting state (white), the second row considers 3-substraction (black) and resting. The two groups (controls and MCIs) are represented in different columns. Only links with p < 0.005 were considered

Fig. 4

Statistical differences in connectivity between controls and MCIs in resting state and 3-substraction task. Significantly altered links (p < 0.02) are shown for every frequency band. A line between two nodes represents a link that has been significantly altered and is either increased (MCI > control) or decreased (control > MCI) in the MCI group. As in Fig. 2, for clarity in visualization, loose links were removed and a maximum of 150 links was displayed