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.
Project description:The coordination of movement between the upper limbs is a function highly distributed across the animal kingdom. How the central nervous system generates such bilateral, synchronous movements, and how this differs from the generation of unilateral movements, remain uncertain. Electrophysiologic and functional imaging studies support that the activity of many brain regions during bimanual and unimanual movement is quite similar. Thus, the same brain regions (and indeed the same neurons) respond similarly during unimanual and bimanual movements as measured by electrophysiological responses. How then are different motor behaviors generated? To address this question, we studied unimanual and bimanual movements using fMRI and constructed networks of activation using Structural Equation Modeling (SEM). Our results suggest that (1) the dominant hemisphere appears to initiate activity responsible for bimanual movement; (2) activation during bimanual movement does not reflect the sum of right and left unimanual activation; (3) production of unimanual movement involves a network that is distinct from, and not a mirror of, the network for contralateral unimanual movement; and (4) using SEM, it is possible to obtain robust group networks representative of a population and to identify individual networks which can be used to detect subtle differences both between subjects as well as within a single subject over time. In summary, these results highlight a differential role for the dominant and non-dominant hemispheres during bimanual movements, further elaborating the concept of handedness and dominance. This knowledge increases our understanding of cortical motor physiology in health and after neurological damage.
Project description: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.
Project description:Our objective was to delineate components of motor performance in specific language impairment (SLI); specifically, whether deficits in timing precision in one effector (unimanual tapping) and in two effectors (bimanual clapping) are observed in young children with SLI.Twenty-seven 4- to 5-year-old children with SLI and 21 age-matched peers with typical language development participated. All children engaged in a unimanual tapping and a bimanual clapping timing task. Standard measures of language and motor performance were also obtained.No group differences in timing variability were observed in the unimanual tapping task. However, compared with typically developing peers, children with SLI were more variable in their timing precision in the bimanual clapping task. Nine of the children with SLI performed greater than 1 SD below the mean on a standardized motor assessment. The children with low motor performance showed the same profile as observed across all children with SLI, with unaffected unimanual and impaired bimanual timing precision.Although unimanual timing is unaffected, children with SLI show a deficit in timing that requires bimanual coordination. We propose that the timing deficits observed in children with SLI are associated with the increased demands inherent in bimanual performance.
Project description:Motor learning in unimanual and bimanual planar reaching movements has been intensively investigated. Although distinct theoretical frameworks have been proposed for each of these reaching movements, the relationship between these movements remains unclear. In particular, the generalization of motor learning effects (transfer of learning effects) between unimanual and bimanual movements has yet to be successfully explained. Here, by extending a motor primitive framework, we analytically proved that the motor primitive framework can reproduce the generalization of learning effects between unimanual and bimanual movements if the mean activity of each primitive for unimanual movements is balanced to the mean for bimanual movements. In this balanced condition, the activity of each primitive is consistent with previously reported neuronal activity. The unimanual-bimanual balance leads to the testable prediction that generalization between unimanual and bimanual movements is more widespread to different reaching directions than generalization within respective movements. Furthermore, the balanced motor primitive can reproduce another previously reported phenomenon: the learning of different force fields for unimanual and bimanual movements.
Project description:Reaching and grasping (prehension) is one of the earliest developing motor skills in humans, but continued prehension development in childhood and adolescence enables the performance of increasingly complex manual tasks. In individuals with autism spectrum disorder (ASD) atypical unimanual reaching and grasping has been reported, but to date, no studies have investigated discrete bimanual movements. We examined unimanual and bimanual reach to grasp tasks in youth with ASD to better understand how motor performance might change with increasing complexity. Twenty youth with ASD (10.1 ± 2.4 years) and 17 youth with typical development (TD) (9.6 ± 2.6 years) were instructed to reach and grasp cubes that became illuminated. Participants were asked to reach out with the right and/or left hands to grasp and lift targets located at near (18 cm) and/or far (28 cm) distances. For the unimanual (simplest) condition, participants grasped one illuminated cube (with either the left or right hand). For the bimanual conditions, participants grasped two illuminated cubes located at the same distance from the start position (bimanual symmetric condition) or two illuminated cubes located at different distances (bimanual asymmetric condition). Significant interactions among diagnostic group, task complexity, and age were found for initiation time (IT) and movement time (MT). Specifically, the older children in both groups initiated and performed their movements faster in the unimanual condition than in the bimanual conditions, although the older children with ASD produced slower ITs and MTs compared to typically developing peers across all three conditions. Surprisingly, the younger children with ASD had similar ITs and MTs as their peers for the unimanual condition but did not considerably slow these times to adjust for the complexity of the bimanual tasks. We hypothesize that they chose to re-use the motor plans that were generated for the unimanual trials rather than generate more appropriate motor plans for the bimanual tasks. An atypical spatiotemporal relationship between MT and peak aperture (PA) was also found in the ASD group. Together, our results suggest deficits in motor planning that result in subtle effects on performance in younger children with ASD that become more pronounced with age.
Project description:The execution of coordinated hand movements requires complex interactions between premotor and primary motor areas in the two hemispheres. The supplementary motor area (SMA) is involved in movement preparation and bimanual coordination. How the SMA controls bimanual coordination remains unclear, although there is evidence suggesting that the SMA could modulate interhemispheric interactions. With a delayed-response task, we investigated interhemispheric interactions underlying normal movement preparation and the role of the SMA in these interactions during the delay period of unimanual or bimanual hand movements. We used functional MRI and transcranial magnetic stimulation in 22 healthy volunteers (HVs), and then in two models of SMA dysfunction: (a) in the same group of HVs after transient disruption of the right SMA proper by continuous transcranial magnetic theta-burst stimulation; (b) in a group of 22 patients with congenital mirror movements (CMM), whose inability to produce asymmetric hand movements is associated with SMA dysfunction. In HVs, interhemispheric connectivity during the delay period was modulated according to whether or not hand coordination was required for the forthcoming movement. In HVs following SMA disruption and in CMM patients, interhemispheric connectivity was modified during the delay period and the interhemispheric inhibition was decreased. Using two models of SMA dysfunction, we showed that the SMA modulates interhemispheric interactions during movement preparation. This unveils a new role for the SMA and highlights its importance in coordinated movement preparation.
Project description:Manual action verbs modulate the right-hand grip force in right-handed subjects. However, to our knowledge, no studies demonstrate the ability to accomplish this modulation during bimanual tasks nor describe their effect on left-hand behavior in unimanual and bimanual tasks. Using load cells and word playlists, we evaluated the occurrence of grip force modulation by manual action verbs in unimanual and symmetrical bimanual tasks across the three auditory processing phases. We found a significant grip force increase for all conditions compared to baseline, indicating the occurrence of modulation. When compared to each other, the grip force variation from baseline for the three phases of both hands in the symmetrical bimanual task was not different from the right-hand in the unimanual task. The left-hand grip force showed a lower amplitude for auditory phases 1 and 2 when compared to the other conditions. The right-hand grip force modulation became significant from baseline at 220 ms after the word onset in the unimanual task. This moment occurred earlier for both hands in bimanual task (160 ms for the right-hand and 180 for the left-hand). It occurred later for the left-hand in unimanual task (320 ms). We discuss the hypothesis that Broca's area and Broca's homologue area likely control the left-hand modulation in a unilateral or a bilateral fashion. These results provide new evidence for understanding the linguistic function processing in both hemispheres.
Project description:The aims of this study were twofold: first, to develop and validate a timed test of unimanual and bimanual dexterity suitable for those with disability affecting hand function; second, to explore relationships between unimanual and bimanual completion times.We developed the Tyneside Pegboard Test (TPT), an electronically timed test with three peg sizes, incorporating an asymmetrical bimanual task. Nine hundred and seventy-four participants (455 males, 519 females; age range 4-80y) provided normative data. Test-retest reliability and construct validity were assessed (50 adults: 14 males, 36 females; 15-73y) on two occasions 2 weeks apart. Bimanual and unimanual completion times were measured in 87 children (51 males, 36 females) with unilateral cerebral palsy (CP) and 498 individuals in a comparison group (238 males, 260 females; 5-15y).The comparison group showed an asymmetrical U-shaped relationship between completion times and age. Intraclass correlation coefficients ranged from 0.74 to 0.91, indicating moderate test-retest reliability. There was a negative relationship between average TPT bimanual times and Purdue pegboard bimanual scores (Spearman's rho -0.611, degrees of freedom 44, p<0.001). Children with unilateral CP had greater prolongation of bimanual than unimanual completion times compared with the comparison group (mean difference 20.31s, 95% confidence interval 18.13-22.49, p<0.001).The TPT is accessible for those with impaired hand function. Children with unilateral CP demonstrated disproportionate bimanual deficits, even allowing for unimanual dexterity: this has implications for therapy.We developed an adapted, electronically timed 9-hole pegboard test. Our modifications facilitate use by those with disability affecting hand function. The test incorporates an asymmetrical bimanual task. Children with unilateral cerebral palsy showed disproportionate bimanual dexterity deficits even allowing for unimanual dexterity.
Project description:Older adults exhibit more bilateral motor cortical activity during unimanual task performance than young adults. Interestingly, a similar pattern is seen in young adults with reduced hand dominance. However, older adults report stronger hand dominance than young adults, making it unclear how handedness is manifested in the aging motor cortex. Here, we investigated age differences in the relationships between handedness, motor cortical organization, and interhemispheric communication speed. We hypothesized that relationships between these variables would differ for young and older adults, consistent with our recent proposal of an age-related shift in interhemispheric interactions. We mapped motor cortical representations of the right and left first dorsal interosseous muscles using transcranial magnetic stimulation (TMS) in young and older adults recruited to represent a broad range of the handedness spectrum. We also measured interhemispheric communication speed and bimanual coordination. We observed that more strongly handed older adults exhibited more ipsilateral motor activity in response to TMS; this effect was not present in young adults. Furthermore, we found opposing relationships between interhemispheric communication speed and bimanual performance in the two age groups. Thus, handedness manifests itself differently in the motor cortices of young and older adults and has interactive effects with age.
Project description:Background:Noisy galvanic vestibular stimulation (nGVS) has been shown to improve motor performance in people with and without disabilities. Previous investigations on the use of nGVS to improve upper-limb motor performance have focused on unimanual fine motor movements, nevertheless, bimanual gross movements are also essential for conducting activities of daily living and can be affected as a result of cerebral dysfunction. Consequently, in this study we investigated the effects of nGVS on bimanual gross motor performance. Methods:Twelve healthy participants completed a visuomotor task in which they performed bimanual upper-limb movements using two robots. During the task, participants tracked a target that oscillated following a sinusoidal amplitude-modulated trajectory. In half of the trials, participants received subthreshold nGVS, in the other half, they received sham stimulation. Primary outcome measure: percent improvement in root mean square error (RMSE) between the target's and cursors' trajectories. Secondary outcome measures: percent improvement in lag between the cursors and target; and percent improvement in RMSE between the cursors' trajectories. A post-test questionnaire was administered to evaluate the experience of participants. Results:Tracking error was not affected by nGVS: left -2.6(5.5)%, p = 0.128; right -0.9(6.2)%, p = 0.639; nor was bimanual coordination -1.5(9.6)%, p = 0.590. When comparing if one hand was affected more than the other, we did not find a statistically significant difference (-1.7(3.3)%, p = 0.098). Similar results were found for the lag. Questionnaire results indicated that the robotic devices did not limit participants' movements, did not make participants feel unsafe, nor were they difficult to control. Furthermore, participants did not feel unsafe with the nGVS device, nor did they report any discomfort due to nGVS. Conclusion:Results suggest that nGVS applied to people without disabilities do not affect bimanual gross motor performance. However, as this was the first study to investigate such effects, stimulation parameters were based on previous unimanual fine motor studies. Future studies should investigate optimal stimulation parameters for improving upper-limb gross motor performance. Overall, participants felt safe using the robotic devices and receiving the noisy electrical stimulation. As such, a similar setup could potentially be employed for subsequent studies investigating the relation between upper-limb performance and nGVS.