Aging-associated changes of movement-related functional connectivity in the human brain

Abstract

Motor performance declines with normal aging. Previous neuroimaging work revealed aging-related general increases in neural activity, especially in the prefrontal and pre-motor areas, associated with a loss of hemispheric lateralization. However, the functional mechanisms underlying these changes and their relation to aging-associated motor decline to date remain elusive. To further elucidate the neural processes underlying aging-related motor decline, we recorded EEG from younger and older subjects while they performed a finger-tapping task. As a measure of synchronization between motor areas, we computed the inter-regional phase-locking value which reflects functional connectivity between distinct neural populations. Behavioral data revealed increased movement times in older subjects. EEG data showed that phase locking in the δ-θ frequencies is a general, age-independent phenomenon underlying the execution of simple finger movements. In stark contrast, the extent of synchronization between motor areas significantly differed dependent upon age of subjects: multiple additional intra- and inter-hemispheric connections were observed in older subjects. Our data shed light upon the results of previous neuroimaging studies showing aging-related increases in neural activation. In particular, data suggest that the observed aging-dependent substantial intra- and inter-hemispheric reorganization of connectivity between the corresponding motor areas underlies the previously reported loss of lateralization in older subjects. The changes observed are likely to represent compensatory mechanisms aiming at preserved task performance in older subjects.

Stimulus transformation into motor action: dynamic graph analysis reveals a posterior-to-anterior shift in brain network communication of older subjects

“…Several studies using data from EEG/MEG/single-unit/ECog recordings while subjects performed a variety of different motor tasks showed that remote neural populations synchronize over a short-time period (Singer, 1999(Singer, , 2004Uhlhaas, Roux, Rodriguez, Rotarska-Jagiela, & Singer, 2010;van Wijk, Beek, & Daffertshofer, 2012), suggesting that coordinated timing constitutes a fundamental principle involved in motor and cognitive processing (Uhlhaas et al, 2010;Fries, 2005Fries, , 2015Baker, Olivier, & Lemon, 1997;Baker, Spinks, Jackson, & Lemon, 2001). Furthermore, we could show in a previous study (Rosjat et al, 2018) that during voluntary, i.e. internally-triggered movements, motor-related networks built on inter-regional neural synchronization in the lower frequencies in younger as well as older subjects.…”

“…Third, we wanted to analyze whether the neural evidence for the HAROLD model found in voluntary, i.e. self-initiated movements (Rosjat et al, 2018) could be replicated in visually-cued movements, i.e. whether the neural underpinnings are independent of the way the movement was initiated.…”

“…1 (A) and (B)) and the conditions were analyzed locked to the onset of the visual stimulus. We used the same cohort as 5/30 in (Rosjat et al, 2018) for the following reason. We wanted to check whether the type of movement initiation (internal versus external) has an influence on the observed coupling structure.…”

“…For the construction of the rPLV networks, we defined a connection, i.e., an edge of the network, between two given nodes to exist at a given time point t if the mean rPLV between these two nodes was significantly increased with respect to its baseline value. Based on our previous results (Rosjat et al, 2018;Popovych et al, 2016), which showed a symmetrical behavior of phase-locking, and to reduce the number of statistical comparisons, the rPLVs during left-and right-hand finger movements were collapsed together after flipping the ones for the right-hand movements. Electrodes were defined as being either ipsilateral or contralateral to the moved hand.…”

“…Aggregated networks In the following, we investigated the aggregated networks, in order compare the results presented here on visually-cued movements, with the already published results of the analyses on self-initiated movements (Rosjat et al, 2018), as these had a much lower time resolution. The resulting networks are presented in Fig.…”