Abstract
Several theories of cognitive compensation have been suggested to explain sustained cognitive abilities in healthy brain aging and early neurodegenerative processes. The growing number of studies investigating various aspects of task-based compensation in these conditions is contrasted by the shortage of data about resting-state compensatory mechanisms. Using our proposed criterion-based framework for compensation, we investigated 45 participants in three groups: (i) patients with mild cognitive impairment (MCI) and positive biomarkers indicative of Alzheimer’s disease (AD); (ii) cognitively normal young adults; (iii) cognitively normal older adults. To increase reliability, three sessions of resting-state functional magnetic resonance imaging for each participant were performed on different days (135 scans in total). To elucidate the dimensions and dynamics of resting-state compensatory mechanisms, we used graph theory analysis along with volumetric analysis. Graph theory analysis was applied based on the Brainnetome atlas, which provides a connectivity-based parcellation framework. Comprehensive neuropsychological examinations including the Rey Auditory Verbal Learning Test (RAVLT) and the Trail Making Test (TMT) were performed, to relate graph measures of compensatory nodes to cognition. To avoid false-positive findings, results were corrected for multiple comparisons. First, we observed an increase of degree centrality in cognition related brain regions of the middle frontal gyrus, precentral gyrus and superior parietal lobe despite local atrophy in MCI and healthy aging, indicating a resting-state connectivity increase with positive biomarkers. When relating the degree centrality measures to cognitive performance, we observed that greater connectivity led to better RAVLT and TMT scores in MCI and, hence, might constitute a compensatory mechanism. The detection and improved understanding of the compensatory dynamics in healthy aging and prodromal AD is mandatory for implementing and tailoring preventive interventions aiming at preserved overall cognitive functioning and delayed clinical onset of dementia.
Highlights
Opposing effects of aging on brain functions have been reported: elderly individuals show decreased activity in some brain regions but increased activity in others (Cabeza and Dennis, 2012)
We observed an increase of degree centrality (DC) in the senior HC and mild cognitive impairment (MCI) group vs. young HC in three ROIs: the right superior parietal lobule, rostral area 7 (Brainnetome label: SPL_R_5_1), the right and left precentral gyri caudal dorsolateral area 6 (Brainnetome label: PrG_R_6_2 and PrG_L_6_2) (Figures 2A,C, 3A, increases of DC depicted in circles of blue shades, decreases in red shades; see Table 2)
The comparison between the senior HC and the MCI group revealed an increase of DC in the right middle frontal gyrus, lateral areal 10 (Brainnetome label: MFG_R_7_7) (Figures 2B,C, 3A and Table 2)
Summary
Opposing effects of aging on brain functions have been reported: elderly individuals show decreased activity in some brain regions but increased activity in others (Cabeza and Dennis, 2012). Contrary to the initial belief, these and other studies have shown that “neuroplasticity” is not solely confined to children (Dennis et al, 2013) but is observable in the healthy aging brain (Fuchs and Flügge, 2014) and even under the circumstances of neurodegeneration (Enciu et al, 2011), including Alzheimer’s Disease (delEtoile and Adeli, 2017). The latter findings gave rise to the concept of “neuronal compensation.”. Resting-state studies offer several advantages over task-based ones, as they place low demands on the experimental design, compliance, instructions to be followed by participants, and training demands
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