Age-Dependent Modulations of Resting State Connectivity Following Motor Practice.

Recent work in young adults has demonstrated that motor learning can modulate resting state functional connectivity. However, evidence for older adults is scarce. Here, we investigated whether learning a bimanual tracking task modulates resting state functional connectivity of both inter- and intra-hemispheric regions differentially in young and older individuals, and whether this has behavioral relevance. Both age groups learned a set of complex bimanual tracking task variants over a 2-week training period. Resting-state and task-related functional magnetic resonance imaging scans were collected before and after training. Our analyses revealed that both young and older adults reached considerable performance gains. Older adults even obtained larger training-induced improvements relative to baseline, but their overall performance levels were lower than in young adults. Short-term practice resulted in a modulation of resting state functional connectivity, leading to connectivity increases in young adults, but connectivity decreases in older adults. This pattern of age differences occurred for both inter- and intra-hemispheric connections related to the motor network. Additionally, long-term training-induced increases were observed in intra-hemispheric connectivity in the right hemisphere across both age groups. Overall, at the individual level, the long-term changes in inter-hemispheric connectivity correlated with training-induced motor improvement. Our findings confirm that short-term task practice shapes spontaneous brain activity differentially in young and older individuals. Importantly, the association between changes in resting state functional connectivity and improvements in motor performance at the individual level may be indicative of how training shapes the short-term functional reorganization of the resting state motor network for improvement of behavioral performance.

White matter microstructural organisation of interhemispheric pathways predicts different stages of bimanual coordination learning in young and older adults.

The ability to learn new motor skills is crucial for activities of daily living, especially in older adults. Previous work in younger adults has indicated fast and slow stages for motor learning that were associated with changes in functional interactions within and between brain hemispheres. However, the impact of the structural scaffolds of these functional interactions on different stages of motor learning remains elusive. Using diffusion-weighted imaging and probabilistic constrained spherical deconvolution-based tractography, we reconstructed transcallosal white matter pathways between the left and right primary motor cortices (M1-M1), left dorsal premotor cortex and right primary motor cortex (LPMd-RM1) and right dorsal premotor cortex and left primary motor cortex (RPMd-LM1) in younger and older adults trained in a set of bimanual coordination tasks. We used fractional anisotropy (FA) to assess microstructural organisation of the reconstructed white matter pathways. Older adults showed lower behavioural performance than younger adults and improved their performance more in the fast but less in the slow stage of learning. Linear mixed models predicted that individuals with higher FA of M1-M1 pathways improve more in the fast but less in the slow stage of bimanual learning. Individuals with higher FA of RPMd-LM1 improve more in the slow but less in the fast stage of bimanual learning. These predictions did not differ significantly between younger and older adults suggesting that, in both younger and older adults, the M1-M1 and RPMd-LM1 pathways are important for the fast and slow stage of bimanual learning, respectively.

Anatomy of Subcortical Structures Predicts Age-Related Differences in Skill Acquisition.

Skill acquisition capabilities vary substantially from one individual to another. Volumetric brain studies have demonstrated that global volume of several subcortical structures predicts variations in learning outcome in young adults (YA) and older adults (OA). In this study, for the first time, we utilized shape analysis, which offers a more sensitive detection of subregional brain anatomical deformations, to investigate whether subregional anatomy of subcortical structures is associated with training-induced performance improvement on a bimanual task in YA and OA, and whether this association is age-dependent. Compared with YA, OA showed poorer performance, greater performance improvement, and smaller global volume and compressed subregional shape in subcortical structures. In OA, global volume of the right nucleus accumbens and subregional shape of the right thalamus, caudate, putamen and nucleus accumbens were positively correlated with acquisition of difficult (non-preferred) but not easy (preferred) task conditions. In YA, global volume and subregional shape of the right hippocampus were negatively correlated with performance improvement in both the easy and difficult conditions. We argue that pre-existing neuroanatomical measures of subcortical structures involved in motor learning differentially predict skill acquisition potential in YA and OA.

Relative cortico-subcortical shift in brain activity but preserved training-induced neural modulation in older adults during bimanual motor learning.

To study age-related differences in neural activation during motor learning, functional magnetic resonance imaging scans were acquired from 25 young (mean 21.5-year old) and 18 older adults (mean 68.6-year old) while performing a bimanual coordination task before (pretest) and after (posttest) a 2-week training intervention on the task. We studied whether task-related brain activity and training-induced brain activation changes differed between age groups, particularly with respect to the hyperactivation typically observed in older adults. Findings revealed that older adults showed lower performance levels than younger adults but similar learning capability. At the cerebral level, the task-related hyperactivation in parietofrontal areas and underactivation in subcortical areas observed in older adults were not differentially modulated by the training intervention. However, brain activity related to task planning and execution decreased from pretest to posttest in temporo-parieto-frontal areas and subcortical areas in both age groups, suggesting similar processes of enhanced activation efficiency with advanced skill level. Furthermore, older adults who displayed higher activity in prefrontal regions at pretest demonstrated larger training-induced performance gains. In conclusion, in spite of prominent age-related brain activation differences during movement planning and execution, the mechanisms of learning-related reduction of brain activation appear to be similar in both groups. Importantly, cerebral activity during early learning can differentially predict the amplitude of the training-induced performance benefit between young and older adults.

Movement preparation and execution: differential functional activation patterns after traumatic brain injury.

Years following the insult, patients with traumatic brain injury often experience persistent motor control problems, including bimanual coordination deficits. Previous studies revealed that such deficits are related to brain structural white and grey matter abnormalities. Here, we assessed, for the first time, cerebral functional activation patterns during bimanual movement preparation and performance in patients with traumatic brain injury, using functional magnetic resonance imaging. Eighteen patients with moderate-to-severe traumatic brain injury (10 females; aged 26.3 years, standard deviation = 5.2; age range: 18.4-34.6 years) and 26 healthy young adults (15 females; aged 23.6 years, standard deviation = 3.8; age range: 19.5-33 years) performed a complex bimanual tracking task, divided into a preparation (2 s) and execution (9 s) phase, and executed either in the presence or absence of augmented visual feedback. Performance on the bimanual tracking task, expressed as the average target error, was impaired for patients as compared to controls (P < 0.001) and for trials in the absence as compared to the presence of augmented visual feedback (P < 0.001). At the cerebral level, movement preparation was characterized by reduced neural activation in the patient group relative to the control group in frontal (bilateral superior frontal gyrus, right dorsolateral prefrontal cortex), parietal (left inferior parietal lobe) and occipital (right striate and extrastriate visual cortex) areas (P's < 0.05). During the execution phase, however, the opposite pattern emerged, i.e. traumatic brain injury patients showed enhanced activations compared with controls in frontal (left dorsolateral prefrontal cortex, left lateral anterior prefrontal cortex, and left orbitofrontal cortex), parietal (bilateral inferior parietal lobe, bilateral superior parietal lobe, right precuneus, right primary somatosensory cortex), occipital (right striate and extrastriate visual cortices), and subcortical (left cerebellum crus II) areas (P's < 0.05). Moreover, a significant interaction effect between Feedback Condition and Group in the primary motor area (bilaterally) (P < 0.001), the cerebellum (left) (P < 0.001) and caudate (left) (P < 0.05), revealed that controls showed less overlap of activation patterns accompanying the two feedback conditions than patients with traumatic brain injury (i.e. decreased neural differentiation). In sum, our findings point towards poorer predictive control in traumatic brain injury patients in comparison to controls. Moreover, irrespective of the feedback condition, overactivations were observed in traumatically brain injured patients during movement execution, pointing to more controlled processing of motor task performance.

Challenge to promote change: both young and older adults benefit from contextual interference.

Current society has to deal with major challenges related to our constantly increasing population of older adults. Since, motor performance generally deteriorates at older age, research investigating the effects of different types of training on motor improvement is particularly important. Here, we tested the effects of contextual interference (CI) while learning a bimanual coordination task in both young and older subjects. Both age groups acquired a low and high complexity task variant following either a blocked or random practice schedule. Typical CI effects, i.e., better overall performance during acquisition but detrimental effects during retention for the blocked compared with the random groups, were found for the low complexity task variant in both age groups. With respect to the high complexity task variant, no retention differences between both practice schedules were found. However, following random practice, better skill persistence (i.e., from end of acquisition to retention) over a 1 week time interval was observed for both task complexity variants and in both age groups. The current study provides clear evidence that the effects of different practice schedules on learning a complex bimanual task are not modulated by age.

Reduced Neural Differentiation Between Feedback Conditions After Bimanual Coordination Training with and without Augmented Visual Feedback.

It has been established that bimanual coordination with augmented feedback (FB) versus no augmented feedback (NFB) is associated with activity in different brain regions. It is unclear however, whether this distinction remains after practice comprising both these conditions. Functional magnetic resonance imaging was used in humans to compare visual FB versus NFB conditions for a bimanual tracking task, and their differential evolution across learning. Scanning occurred before (Pre) and after 2 weeks (Post) of mixed FB and NFB training using an event-related design, allowing differentiation between the planning and execution phase of the task. Activations at the whole-brain level initially differed for FB versus NFB movements but this differentiation diminished with training for the movement execution phase. Specifically, in right dorsal premotor cortex and right dorsolateral prefrontal cortex activation increased for NFB and decreased for FB trials to converge toward the end of practice. This suggests that learning led to a decreased need to adjust the ongoing movement on the basis of FB, whereas online monitoring became more pronounced in NFB trials as discrepancies between the required and the produced motor output were detected more accurately after training, due to a generic internal reference of correctness supporting movement control under varying conditions.

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

Despite the intensive investigation of bimanual coordination, it remains unclear how directing vision toward either limb influences performance, and whether this influence is affected by age. To examine these questions, we assessed the performance of young and older adults on a bimanual tracking task in which they matched motor-driven movements of their right hand (passive limb) with their left hand (active limb) according to in-phase and anti-phase patterns. Performance in six visual conditions involving central vision, and/or peripheral vision of the active and/or passive limb was compared to performance in a no vision condition. Results indicated that directing central vision to the active limb consistently impaired performance, with higher impairment in older than young adults. Conversely, directing central vision to the passive limb improved performance in young adults, but less consistently in older adults. In conditions involving central vision of one limb and peripheral vision of the other limb, similar effects were found to those for conditions involving central vision of one limb only. Peripheral vision alone resulted in similar or impaired performance compared to the no vision (NV) condition. These results indicate that the locus of visual attention is critical for bimanual motor control in young and older adults, with older adults being either more impaired or less able to benefit from a given visual condition.

Contextual interference in complex bimanual skill learning leads to better skill persistence.

The contextual interference (CI) effect is a robust phenomenon in the (motor) skill learning literature. However, CI has yielded mixed results in complex task learning. The current study addressed whether the CI effect is generalizable to bimanual skill learning, with a focus on the temporal evolution of memory processes. In contrast to previous studies, an extensive training schedule, distributed across multiple days of practice, was provided. Participants practiced three frequency ratios across three practice days following either a blocked or random practice schedule. During the acquisition phase, better overall performance for the blocked practice group was observed, but this difference diminished as practice progressed. At immediate and delayed retention, the random practice group outperformed the blocked practice group, except for the most difficult frequency ratio. Our main finding is that the random practice group showed superior performance persistence over a one week time interval in all three frequency ratios compared to the blocked practice group. This study contributes to our understanding of learning, consolidation and memory of complex motor skills, which helps optimizing training protocols in future studies and rehabilitation settings.

Aging effects on the resting state motor network and interlimb coordination.

Both increases and decreases in resting state functional connectivity have been previously observed within the motor network during aging. Moreover, the relationship between altered functional connectivity and age-related declines in bimanual coordination remains unclear. Here, we explored the developmental dynamics of the resting brain within a task-specific motor network in a sample of 128 healthy participants, aged 18-80 years. We found that age-related increases in functional connectivity between interhemispheric dorsal and ventral premotor areas were associated with poorer performance on a novel bimanual visuomotor task. Additionally, a control analysis performed on the default mode network confirmed that our age-related increases in functional connectivity were specific to the motor system. Our findings suggest that increases in functional connectivity within the resting state motor network with aging reflect a loss of functional specialization that may not only occur in the active brain but also in the resting brain.

Age-related differences in attentional cost associated with postural dual tasks: increased recruitment of generic cognitive resources in older adults.

Dual-task designs have been used widely to study the degree of automatic and controlled processing involved in postural stability of young and older adults. However, several unexplained discrepancies in the results weaken this literature. To resolve this problem, a careful selection of dual-task studies that met certain methodological criteria are considered with respect to reported interactions of age (young vs. older adults)×task (single vs. dual task) in stable and unstable postural conditions. Our review shows that older adults are able to perform a postural dual task as well as younger adults in stable conditions. However, when the complexity of the postural task is increased by dynamic conditions (surface and surround), performance in postural, concurrent, or both tasks is more affected in older relative to young adults. In light of neuroimaging studies and new conceptual frameworks, these results demonstrate an age-related increase of controlled processing of standing associated with greater intermittent adjustments.

Microstructural organization of corpus callosum projections to prefrontal cortex predicts bimanual motor learning.

The corpus callosum (CC) is the largest white matter tract in the brain. It enables interhemispheric communication, particularly with respect to bimanual coordination. Here, we use diffusion tensor imaging (DTI) in healthy humans to determine the extent to which structural organization of subregions within the CC would predict how well subjects learn a novel bimanual task. A single DTI scan was taken prior to training. Participants then practiced a bimanual visuomotor task over the course of 2 wk, consisting of multiple coordination patterns. Findings revealed that the predictive power of fractional anisotropy (FA) was a function of CC subregion and practice. That is, FA of the anterior CC, which projects to the prefrontal cortex, predicted bimanual learning rather than the middle CC regions, which connect primary motor cortex. This correlation was specific in that FA correlated significantly with performance of the most difficult frequency ratios tested and not the innately preferred, isochronous frequency ratio. Moreover, the effect was only evident after training and not at initiation of practice. This is the first DTI study in healthy adults which demonstrates that white matter organization of the interhemispheric connections between the prefrontal structures is strongly correlated with motor learning capability.

Active versus passive training of a complex bimanual task: is prescriptive proprioceptive information sufficient for inducing motor learning?

Perceptual processes play an important role in motor learning. While it is evident that visual information greatly contributes to learning new movements, much less is known about provision of prescriptive proprioceptive information. Here, we investigated whether passive (proprioceptively-based) movement training was comparable to active training for learning a new bimanual task. Three groups practiced a bimanual coordination pattern with a 1:2 frequency ratio and a 90° phase offset between both wrists with Lissajous feedback over the course of four days: 1) passive training; 2) active training; 3) no training (control). Retention findings revealed that passive as compared to active training resulted in equally successful acquisition of the frequency ratio but active training was more effective for acquisition of the new relative phasing between the limbs in the presence of augmented visual feedback. However, when this feedback was removed, performance of the new relative phase deteriorated in both groups whereas the frequency ratio was better preserved. The superiority of active over passive training in the presence of augmented feedback is hypothesized to result from active involvement in processes of error detection/correction and planning.

Testing multiple coordination constraints with a novel bimanual visuomotor task.

The acquisition of a new bimanual skill depends on several motor coordination constraints. To date, coordination constraints have often been tested relatively independently of one another, particularly with respect to isofrequency and multifrequency rhythms. Here, we used a new paradigm to test the interaction of multiple coordination constraints. Coordination constraints that were tested included temporal complexity, directionality, muscle grouping, and hand dominance. Twenty-two healthy young adults performed a bimanual dial rotation task that required left and right hand coordination to track a moving target on a computer monitor. Two groups were compared, either with or without four days of practice with augmented visual feedback. Four directional patterns were tested such that both hands moved either rightward (clockwise), leftward (counterclockwise), inward or outward relative to each other. Seven frequency ratios (3∶1, 2∶1, 3∶2, 1∶1, 2∶3. 1∶2, 1∶3) between the left and right hand were introduced. As expected, isofrequency patterns (1∶1) were performed more successfully than multifrequency patterns (non 1∶1). In addition, performance was more accurate when participants were required to move faster with the dominant right hand (1∶3, 1∶2 and 2∶3) than with the non-dominant left hand (3∶1, 2∶1, 3∶2). Interestingly, performance deteriorated as the relative angular velocity between the two hands increased, regardless of whether the required frequency ratio was an integer or non-integer. This contrasted with previous finger tapping research where the integer ratios generally led to less error than the non-integer ratios. We suggest that this is due to the different movement topologies that are required of each paradigm. Overall, we found that this visuomotor task was useful for testing the interaction of multiple coordination constraints as well as the release from these constraints with practice in the presence of augmented visual feedback.

Neural competition for conscious representation across time: an fMRI study.

BACKGROUND: The information processing capacity of the human mind is limited, as is evidenced by the attentional blink (AB)--a deficit in identifying the second of two temporally-close targets (T1 and T2) embedded in a rapid stream of distracters. Theories of the AB generally agree that it results from competition between stimuli for conscious representation. However, they disagree in the specific mechanisms, in particular about how attentional processing of T1 determines the AB to T2. METHODOLOGY/PRINCIPAL FINDINGS: The present study used the high spatial resolution of functional magnetic resonance imaging (fMRI) to examine the neural mechanisms underlying the AB. Our research approach was to design T1 and T2 stimuli that activate distinguishable brain areas involved in visual categorization and representation. ROI and functional connectivity analyses were then used to examine how attentional processing of T1, as indexed by activity in the T1 representation area, affected T2 processing. Our main finding was that attentional processing of T1 at the level of the visual cortex predicted T2 detection rates Those individuals who activated the T1 encoding area more strongly in blink versus no-blink trials generally detected T2 on a lower percentage of trials. The coupling of activity between T1 and T2 representation areas did not vary as a function of conscious T2 perception. CONCLUSIONS/SIGNIFICANCE: These data are consistent with the notion that the AB is related to attentional demands of T1 for selection, and indicate that these demands are reflected at the level of visual cortex. They also highlight the importance of individual differences in attentional settings in explaining AB task performance.