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Cooperation Not Competition: Bihemispheric tDCS and fMRI Show Role for Ipsilateral Hemisphere in Motor Learning.

ABSTRACT: What is the role of ipsilateral motor and premotor areas in motor learning? One view is that ipsilateral activity suppresses contralateral motor cortex and, accordingly, that inhibiting ipsilateral regions can improve motor learning. Alternatively, the ipsilateral motor cortex may play an active role in the control and/or learning of unilateral hand movements. We approached this question by applying double-blind bihemispheric transcranial direct current stimulation (tDCS) over both contralateral and ipsilateral motor cortex in a between-group design during 4 d of unimanual explicit sequence training in human participants. Independently of whether the anode was placed over contralateral or ipsilateral motor cortex, bihemispheric stimulation yielded substantial performance gains relative to unihemispheric or sham stimulation. This performance advantage appeared to be supported by plastic changes in both hemispheres. First, we found that behavioral advantages generalized strongly to the untrained hand, suggesting that tDCS strengthened effector-independent representations. Second, functional imaging during speed-matched execution of trained sequences conducted 48 h after training revealed sustained, polarity-independent increases in activity in both motor cortices relative to the sham group. These results suggest a cooperative rather than competitive interaction of the two motor cortices during skill learning and suggest that bihemispheric brain stimulation during unimanual skill learning may be beneficial because it harnesses plasticity in the ipsilateral hemisphere.SIGNIFICANCE STATEMENT Many neurorehabilitation approaches are based on the idea that is beneficial to boost excitability in the contralateral hemisphere while attenuating that of the ipsilateral cortex to reduce interhemispheric inhibition. We observed that bihemispheric transcranial direct current stimulation (tDCS) with the excitatory anode either over contralateral or ipsilateral motor cortex facilitated motor learning nearly twice as strongly as unihemispheric tDCS. These increases in motor learning were accompanied by increases in fMRI activation in both motor cortices that outlasted the stimulation period, as well as increased generalization to the untrained hand. Collectively, our findings suggest a cooperative rather than a competitive role of the hemispheres and imply that it is most beneficial to harness plasticity in both hemispheres in neurorehabilitation of motor deficits.

SUBMITTER: Waters S

PROVIDER: S-EPMC5546115 | biostudies-other | 2017 Aug

REPOSITORIES: biostudies-other

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Project description:Transcranial direct current stimulation (tDCS) modulates cortical excitability in a polarity-specific way and, when used in combination with a behavioural task, it can alter performance. TDCS has the potential, therefore, for use as an adjunct to therapies designed to treat disorders affecting speech, including, but not limited to acquired aphasias and developmental stuttering. For this reason, it is important to conduct studies evaluating its effectiveness and the parameters optimal for stimulation. Here, we aimed to evaluate the effects of bi-hemispheric tDCS over speech motor cortex on performance of a complex speech motor learning task, namely the repetition of tongue twisters. A previous study in older participants showed that tDCS could modulate performance on a similar task. To further understand the effects of tDCS, we also measured the excitability of the speech motor cortex before and after stimulation. Three groups of 20 healthy young controls received: (i) anodal tDCS to the left IFG/LipM1 and cathodal tDCS to the right hemisphere homologue; or (ii) cathodal tDCS over the left and anodal over the right; or (iii) sham stimulation. Participants heard and repeated novel tongue twisters and matched simple sentences before, during and 10 min after the stimulation. One mA tDCS was delivered concurrent with task performance for 13 min. Motor excitability was measured using transcranial magnetic stimulation to elicit motor-evoked potentials in the lip before and immediately after tDCS. The study was double-blind, randomized, and sham-controlled; the design and analysis were pre-registered. Performance on the task improved from baseline to after stimulation but was not significantly modulated by tDCS. Similarly, a small decrease in motor excitability was seen in all three stimulation groups but did not differ among them and was unrelated to task performance. Bayesian analyses provide substantial evidence in support of the null hypotheses in both cases, namely that tongue twister performance and motor excitability were not affected by tDCS. We discuss our findings in the context of the previous positive results for a similar task. We conclude that tDCS may be most effective when brain function is sub-optimal due to age-related declines or pathology. Further study is required to determine why tDCS failed to modulate excitability in the speech motor cortex in the expected ways.

Project description:Transcranial direct-current stimulation (tDCS) enhances motor learning in adults. We have demonstrated that anodal tDCS and high-definition (HD) tDCS of the motor cortex can enhance motor skill acquisition in children, but behavioral mechanisms remain unknown. Robotics can objectively quantify complex sensorimotor functions to better understand mechanisms of motor learning. We aimed to characterize changes in sensorimotor function induced by tDCS and HD-tDCS paired motor learning in children within an interventional trial. Healthy, right-handed children (12-18?y) were randomized to anodal tDCS, HD-tDCS, or sham targeting the right primary motor cortex during left-hand Purdue pegboard test (PPT) training over five consecutive days. A KINARM robotic protocol quantifying proprioception, kinesthesia, visually guided reaching, and an object hit task was completed at baseline, posttraining, and six weeks later. Effects of the treatment group and training on changes in sensorimotor parameters were explored. Twenty-four children (median 15.5 years, 52% female) completed all measures. Compared to sham, both tDCS and HD-tDCS demonstrated enhanced motor learning with medium effect sizes. At baseline, multiple KINARM measures correlated with PPT performance. Following training, visually guided reaching in all groups was faster and required less corrective movements in the trained arm (H(2)?=?9.250, p = 0.010). Aspects of kinesthesia including initial direction error improved across groups with sustained effects at follow-up (H(2)?=?9.000, p = 0.011). No changes with training or stimulation were observed for position sense. For the object hit task, the HD-tDCS group moved more quickly with the right hand compared to sham at posttraining (? 2(2)?=?6.255, p = 0.044). Robotics can quantify complex sensorimotor function within neuromodulator motor learning trials in children. Correlations with PPT performance suggest that KINARM metrics can assess motor learning effects. Understanding how tDCS and HD-tDCS enhance motor learning may be improved with robotic outcomes though specific mechanisms remain to be defined. Exploring mechanisms of neuromodulation may advance therapeutic approaches in children with cerebral palsy and other disabilities.

Project description:It has been proposed that the cerebellum acquires internal models of mental processes that enable prediction, allowing for the optimization of behavior. In language, semantic prediction speeds speech production and comprehension. Right cerebellar lobules VI and VII (including Crus I/II) are engaged during a variety of language processes and are functionally connected with cerebral cortical language networks. Further, right posterolateral cerebellar neuromodulation modifies behavior during predictive language processing. These data are consistent with a role for the cerebellum in semantic processing and semantic prediction. We combined transcranial direct current stimulation (tDCS) and fMRI to assess the behavioral and neural consequences of cerebellar tDCS during a sentence completion task. Task-based and resting-state fMRI data were acquired in healthy human adults (n = 32; μ = 23.1 years) both before and after 20 min of 1.5 mA anodal (n = 18) or sham (n = 14) tDCS applied to the right posterolateral cerebellum. In the sentence completion task, the first four words of the sentence modulated the predictability of the final target word. In some sentences, the preceding context strongly predicted the target word, whereas other sentences were nonpredictive. Completion of predictive sentences increased activation in right Crus I/II of the cerebellum. Relative to sham tDCS, anodal tDCS increased activation in right Crus I/II during semantic prediction and enhanced resting-state functional connectivity between hubs of the reading/language networks. These results are consistent with a role for the right posterolateral cerebellum beyond motor aspects of language, and suggest that cerebellar internal models of linguistic stimuli support semantic prediction.SIGNIFICANCE STATEMENT Cerebellar involvement in language tasks and language networks is now well established, yet the specific cerebellar contribution to language processing remains unclear. It is thought that the cerebellum acquires internal models of mental processes that enable prediction, allowing for the optimization of behavior. Here we combined neuroimaging and neuromodulation to provide evidence that the cerebellum is specifically involved in semantic prediction during sentence processing. We found that activation within right Crus I/II was enhanced when semantic predictions were made, and we show that modulation of this region with transcranial direct current stimulation alters both activation patterns and functional connectivity within whole-brain language networks. For the first time, these data show that cerebellar neuromodulation impacts activation patterns specifically during predictive language processing.

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Cooperation Not Competition: Bihemispheric tDCS and fMRI Show Role for Ipsilateral Hemisphere in Motor Learning.

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