Distant functional connectivity for bimanual finger coordination declines with aging: an fMRI and SEM exploration

Abstract

Although bimanual finger coordination is known to decline with aging, it still remains unclear how exactly the neural substrates underlying the coordination differ between young and elderly adults. The present study focused on: (1) characterization of the functional connectivity within the motor association cortex which is required for successful bimanual finger coordination, and (2) to elucidate upon its age-related decline. To address these objectives, we utilized functional magnetic resonance imaging (fMRI) in combination with structural equation modeling (SEM). This allowed us to compare functional connectivity models between young and elderly age groups during a visually guided bimanual finger movement task using both stable in-phase and complex anti-phase modes. Our SEM exploration of functional connectivity revealed significant age-related differences in connections surrounding the PMd in the dominant hemisphere. In the young group who generally displayed accurate behavior, the SEM model for the anti-phase mode exhibited significant connections from the dominant PMd to the non-dominant SPL, and from the dominant PMd to the dominant S1. However, the model for the elderly group's anti-phase mode in which task performance dropped, did not exhibit significant connections within the aforementioned regions. These results suggest that: (1) the dominant PMd acts as an intermediary to invoke intense intra- and inter-hemispheric connectivity with distant regions among the higher motor areas including the dominant S1 and the non-dominant SPL in order to achieve successful bimanual finger coordination, and (2) the distant connectivity among the higher motor areas declines with aging, whereas the local connectivity within the bilateral M1 is enhanced for the complex anti-phase mode. The latter may underlie the elderly's decreased performance in the complex anti-phase mode of the bimanual finger movement task.

Subcortical volumetric changes across the adult lifespan: Subregional thalamic atrophy accounts for age-related sensorimotor performance declines

“…Recent aging studies have focused on activity of the cerebral cortex, and have made some progress in determining the role of age-related functional brain changes in bimanual performance declines (Goble et al, 2010;Heitger et al, 2013;Kiyama, Kunimi, Iidaka, & Nakai, 2014;Solesio-Jofre et al, 2014). Other aging studies have demonstrated a significant role of microstructural changes in white matter structures and particularly the corpus callosum (Fling et al, 2011;Gooijers & Swinnen, 2014;Serbruyns et al, 2013;Sullivan et al, 2001), the largest white matter tract connecting interhemispheric cortical regions (Jarbo, Verstynen, & Schneider, 2012).…”

Vision of the active limb impairs bimanual motor tracking in young and older adults

“…This interlimb interference appears to alter with aging. Indeed, studies have demonstrated that bimanual coordination is less accurate and/or more variable in older compared to young adults (Temprado et al, 2010 ; Solesio-Jofre et al, 2014 ), particularly for the anti-phase pattern (Wishart et al, 2000 ; Lee et al, 2002 ; Bangert et al, 2010 ; Summers et al, 2010 ; Fling et al, 2011 ; Kiyama et al, 2014 ). However, this age effect appears to be more pronounced in intermittent than continuous tasks (Bangert et al, 2010 ; Summers et al, 2010 ).…”

Age-related Changes in Bilateral Upper Extremity Coordination

“…Older adults demonstrated increased sensorimotor resting state functional connectivity, in which reductions in bimanual performance strongly related to increases in premotor functional connectivity [68]. Kiyami and colleagues [69] assessed differences in functional connectivity of the sensorimotor network during in-phase and antiphase bilateral finger tapping. In young adults, inter- and intra-hemispheric task-specific connectivity is modulated by left dorsal premotor area (PMd) during in-phase and antiphase tasks.…”

“…In young adults, inter- and intra-hemispheric task-specific connectivity is modulated by left dorsal premotor area (PMd) during in-phase and antiphase tasks. Older adults, in contrast, demonstrated reduced task specific interhemispheric connections of left PMd during both tasks, while intrahemispheric connectivity from left PMd to left M1 was increased during the in-phase task [69]. Given the role of the PMd for motor planning and monitoring, these findings also suggest that older adults may have deficits in these processing stages, rather than motor execution.…”