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Hummel, F. C.

Publications and source records attributed to Hummel, F. C..

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Targeting the fronto-parietal network using multifocal personalized transcranial alternating current stimulation to enhance motor sequence learning in healthy older adults

BackgroundHealthy older adults show a decrease in motor learning capacity as well as in working memory (WM) performance. WM has been suggested to be involved in motor learning processes, such as sequence learning. Correlational evidence has shown the involvement of the fronto-parietal network (FPN), a network underlying WM processes, in motor sequence learning. However, causal evidence is currently lacking. Non-invasive brain stimulation (NIBS) studies have focused so far predominantly on motor related areas to enhance motor sequence learning while areas associated with more cognitive aspects of motor learning have not yet been addressed. HypothesisIn this study, we aim to provide causal evidence for the involvement of WM processes and the underlying FPN in successful motor sequence learning by using a theta transcranial alternating current stimulation (tACS) paradigm targeting the FPN during motor sequence learning. MethodsIn a cohort of 20 healthy older adults, we applied bifocal tACS in the theta range to the FPN during a sequence learning task. With the use of a double-blind, cross-over design, we tested the efficacy of active compared with sham stimulation. Two versions of the motor task were used: one with high and one with low WM load, to explore the efficacy of stimulation on tasks differing in WM demand. Additionally, the effects of stimulation on WM performance were addressed using an N-back task. The tACS frequency was personalized by means of EEG measuring the individual theta peak frequency during the N-back task. ResultsThe application of personalized theta tACS to the FPN improved performance on the motor sequence learning task with high WM load (p <.001), but not with low WM load. Active stimulation significantly improved both speed (p <.001), and accuracy (p =.03) during the task with high WM load. In addition, the stimulation paradigm improved performance on the N-back task for the 2-back task (p = .013), but not for 1-back and 3-back. ConclusionMotor sequence learning can be enhanced with the use of personalized bifocal theta tACS to the FPN when WM load is high. This indicates that the efficacy of this stimulation paradigm is dependent on the cognitive demand during the learning task and provides further causal evidence for the critical involvement of WM processes and the FPN in motor sequence learning in healthy older adults. These findings open new exciting possibilities to counteract the age-related decline in motor learning capacity and WM performance.

neuroscience↗

Black-box testing in motor sequence learning

During learning of novel motor sequences, practice leads to the consolidation of hierarchical structures, namely motor chunks, facilitating the accurate execution of sequences at increasing speeds. Recent studies show that such hierarchical structures are largely represented upstream of the primary motor cortex in the motor network, suggesting their function to be more related to the encoding, storage, and retrieval of sequences rather than their sole execution. We isolated different components of motor skill acquisition related to the consolidation of spatiotemporal features and followed their evolution over training. We found that optimal motor skill acquisition relies on the storage of the spatial features of the sequence in memory, followed by the optimization of its execution and increased execution speeds (i.e., a shift in the speed-accuracy trade-off) early in training, supporting the model proposed by Hikosaka in 1999. Contrasting the dynamics of these components during ageing, we identified less-than-optimal mechanisms in older adults explaining the observed differences in performance. We applied noninvasive brain stimulation in an attempt to support the aging brain to compensate for these deficits. The present study found that anodal direct current stimulation applied over the motor cortex restored the mechanisms involved in the consolidation of spatial features, without directly affecting the speed of execution of the sequence. This led older adults to sharply improve their accuracy, resulting in an earlier yet gradual emergence of motor chunks. The results suggest the early storage of the sequence in memory, largely independent of motor practice, is crucial for an optimal motor acquisition and retrieval of this motor behavior. Nevertheless, the consolidation of optimal temporal patterns, detected as motor chunks at a behavioral level, is not a direct consequence of storing the sequence elements, but rather of motor practice.

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Reward boosts reinforcement-based motor learning

Besides relying heavily on sensory and reinforcement feedback, motor skill learning may also depend on the level of motivation experienced during training. Yet, how motivation by reward modulates motor learning remains unclear. In 90 healthy subjects, we investigated the net effect of motivation by reward on motor learning while controlling for the sensory and reinforcement feedback received by the participants. Reward improved motor skill learning beyond performance-based reinforcement feedback. Importantly, the beneficial effect of reward involved a specific potentiation of reinforcement-related adjustments in motor commands, which concerned primarily the most relevant motor component for task success and persisted on the following day in the absence of reward. We propose that the long-lasting effects of motivation on motor learning may entail a form of associative learning resulting from the repetitive pairing of the reinforcement feedback and reward during training, a mechanism that may be exploited in future rehabilitation protocols.

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Sensory capability and information integration independently predict cognitive status in healthy older adults

Ageing is characterized by changes in sensory and cognitive abilities. While there is evidence that decline in sensory acuity and enhanced multisensory integration predict cognitive status in healthy older adults, potential mechanistic links between these age-related alterations remain unclear. In the current study, we assessed performance of younger and older healthy adults in a visuotactile delayed match-to-sample task and related indices of multisensory integration to unisensory perceptual thresholds and cognitive assessment data. Additionally, we applied transcranial alternating current stimulation (tACS) to modulate cortical networks found to underlie visuotactile interactions and working-memory matching in our previous work. Analysing response times and signal detection measures, we found older adults to show enhanced multisensory integration and benefit more from successful working memory matching. Both measures predicted cognitive status and correlated positively with each other, suggesting that they likely reflect a common underlying tendency to integrate information. Sensory capability, however, independently predicted cognitive status. tACS with beta frequency (20 Hz) accelerated task performance and this effect was more pronounced in the older group. We conclude that sensory capability and information integration represent independent predictors of cognitive status. Finally, we discuss a potential role of the parietal cortex in mediating augmented integration in older adults.

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Congruency effects can compensate for deficits of healthy older adults in crossmodal integration

One of the pivotal challenges of aging is to maintain independence in the activities of daily life. In order to adapt to changes in the environment, it is crucial to continuously process and accurately combine simultaneous input from different sensory systems, i.e., crossmodal integration.\n\nWith aging, performance decreases in multiple cognitive domains. The processing of sensory stimuli constitutes one of the key features of this deterioration. Age-related sensory impairments affect all modalities, substantiated by decreased acuity in visual, auditory or tactile detection tasks.\n\nHowever, whether this decline of sensory processing leads to impairments in crossmodal integration remains an unresolved question. While some researchers propose that crossmodal integration degrades with age, others suggest that it is conserved or even gains compensatory importance.\n\nTo address this question, we compared behavioral performance of older and young participants in a well-established crossmodal matching task, requiring the evaluation of congruency in simultaneously presented visual and tactile patterns. Older participants performed significantly worse than young controls in the crossmodal task when being stimulated at their individual unimodal visual and tactile perception thresholds. Performance increased with adjustment of stimulus intensities. This improvement was driven by better detection of congruent stimulus pairs (p<0.01), while detection of incongruent pairs was not significantly enhanced (p=0.12).\n\nThese results indicate that age-related impairments lead to poor performance in complex crossmodal scenarios and demanding cognitive tasks. Performance is enhanced when inputs to the visual and tactile systems are congruent. Congruency effects might therefore be used to develop strategies for cognitive training and neurological rehabilitation.

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