Functional and effective reorganization of the aging brain during unimanual and bimanual hand movements

Abstract

Motor performance decline observed during aging is linked to changes in brain structure and function, however, the precise neural reorganization associated with these changes remains largely unknown. We investigated the neurophysiological correlates of this reorganization by quantifying functional and effective brain network connectivity in elderly individuals (n = 11; mean age = 67.5 years), compared to young adults (n = 12; mean age = 23.7 years), while they performed visually‐guided unimanual and bimanual handgrips inside the magnetoencephalography (MEG) scanner. Through a combination of principal component analysis and Granger causality, we observed age‐related increases in functional and effective connectivity in whole‐brain, task‐related motor networks. Specifically, elderly individuals demonstrated (i) greater information flow from contralateral parietal and ipsilateral secondary motor regions to the left primary motor cortex during the unimanual task and (ii) decreased interhemispheric temporo‐frontal communication during the bimanual task. Maintenance of motor performance and task accuracy in elderly was achieved by hyperactivation of the task‐specific motor networks, reflecting a possible mechanism by which the aging brain recruits additional resources to counteract known myelo‐ and cytoarchitectural changes. Furthermore, resting‐state sessions acquired before and after each motor task revealed that both older and younger adults maintain the capacity to adapt to task demands via network‐wide increases in functional connectivity. Collectively, our study consolidates functional connectivity and directionality of information flow in systems‐level cortical networks during aging and furthers our understanding of neuronal flexibility in motor processes.

Estimating brain age from structural MRI and MEG data: Insights from dimensionality reduction techniques

“…Finally, we found that AEC measures exhibited an age-related increase in connectivity within all frequency bands across all brain networks, apart from the visual network which showed a decrease in connectivity within the high alpha and high beta frequency bands. These results align well with a recent study where Larivière et al reported lower beta-band connectivity in the visual network and higher beta-band connectivity in all other brain networks with age (Larivière et al, 2019). Higher functional connectivity in older adults has been associated with a lower cognitive reserve (López et al, 2014), and individuals with mild cognitive impairment exhibit an enhancement of the strength of functional connections (Bajo et al, 2010;Buldú et al, 2011).…”

“…It is widely used to decompose multivariate datasets into a set of successive orthogonal components that explain the maximum amount of the data variance (e.g. Amico and Goñi, 2017;Larivière et al, 2019). The obtained principal components correspond to the maximal modes of variation and hence correspond to the most prominently changing features in the dataset.…”

Neural Correlates of Age-Related Changes in Precise Grip Force Regulation: A Combined EEG-fNIRS Study

“…In summary, the older adults showed significant deterioration in grip force control and greater hemodynamic activity during both the FTTs than did the young adults, suggesting a greater computational effort and oxygen supply during the motor tasks (Ward, 2006) which represent a general age-related compensatory mechanism of changes in the sensorimotor network (Noble et al, 2011;Larivière et al, 2019). In contrast, increases in left PMC beta activity that are related to deteriorations in grip force regulation in older adults are task-complexity-dependent, thus representing an increased cognitive effort during motor planning or a compensatory mechanism of deficits in processing the sensory feedback within the sensorimotor network.…”

“…Abbreviations: PMC, premotor cortex; SMC, sensorimotor cortex; r = Pearson correlation coefficient; Significance level p < 0.05 * . Noble et al, 2011;Larivière et al, 2019). Nevertheless, the results of deteriorations in grip force control and higher hemodynamic brain activity in older subjects cannot only be associated with the grip force tasks.…”

“…Thus, it may be possible that age-related decrease in tactile sensibility and the ability to process sensory feedback (Cole et al, 1999 ) lead to declines in grip force control and increased brain activity within the motor-cortical network regardless of the task complexity. Following the compensation theory of aging (Reuter-Lorenz and Park, 2010 ), over-recruitment of cortical resources with aging appears to reflect a greater computational effort and oxygenation owing to compensatory patterns such as reorganization and redistribution of functional networks to counteract age-related structural and neurochemical changes in motor control systems (Bennett and Castiello, 1994 ; Mattay et al, 2002 ; Ward, 2006 ; Noble et al, 2011 ; Larivière et al, 2019 ). Nevertheless, the results of deteriorations in grip force control and higher hemodynamic brain activity in older subjects cannot only be associated with the grip force tasks.…”