Shaping the Sensory–Motor Network by Short-Term Unresolvable Sensory–Motor Mismatch

Learning from errors as the main mechanism for motor adaptation has two fundamental prerequisites: a mismatch between the intended and performed movement and the ability to adapt motor actions. Many neurological patients are limited in their ability to transfer an altered motor representation into motor action due to a compromised motor pathway. Studies that have investigated the effects of a sustained and unresolvable mismatch over multiple days found changes in brain processing that seem to optimize the potential for motor learning (increased drive for motor adaptation and a weakening of the current implementation of motor programs). However, it remains unclear whether the observed effects can be induced experimentally and more important after shorter periods. Here, we used task-based and resting-state fMRI to investigate whether the known pattern of cortical adaptations due to a sustained mismatch can be induced experimentally by a short (20 min), but unresolvable, sensory–motor mismatch by impaired facial movements in healthy participants by transient facial tapping. Similar to long-term mismatch, we found plastic changes in a network that includes the striatal, cerebellar and somatosensory brain areas. However, in contrast to long-term mismatch, we did not find the involvement of the cerebral motor cortex. The lack of the involvement of the motor cortex can be interpreted both as an effect of time and also as an effect of the lack of a reduction in the motor error. The similar effects of long-term and short-term mismatch on other parts of the sensory–motor network suggest that the brain-state caused by long-term mismatch can be (at least partly) induced by short-term mismatch. Further studies should investigate whether short-term mismatch interventions can be used as therapeutic strategy to induce an altered brain-state that increase the potential for motor learning.

Evidence that endpoint feedback facilitates intermanual transfer of visuomotor force learning by a cognitive strategy

Humans continuously adapt their movement to a novel environment by recalibrating their sensorimotor system. Recent evidence, however, shows that explicit planning to compensate for external changes, i.e. a cognitive strategy, can also aid performance. If such a strategy is indeed planned in external space, it should improve performance in an effector independent manner. We tested this hypothesis by examining whether promoting a cognitive strategy during a visual-force adaptation task performed in one hand can facilitate learning for the opposite hand. Participants rapidly adjusted the height of visual bar on screen to a target level by isometrically exerting force on a handle using their right hand. Visuomotor gain increased during the task and participants learned the increased gain. Visual feedback was continuously provided for one group, while for another group only the endpoint of the force trajectory was presented. The latter has been reported to promote cognitive strategy use. We found that endpoint feedback produced stronger intermanual transfer of learning and slower response times than continuous feedback. In a separate experiment, we found evidence that the aftereffect is indeed reduced when only endpoint feedback is provided, a finding that has been consistently observed when cognitive strategies are used. The results suggest that intermanual transfer can be facilitated by a cognitive strategy. This indicates that the behavioral observation of intermanual transfer can be achieved either by forming an effector-independent motor representation, or by sharing an effector-independent cognitive strategy between the hands.

Combining Optogenetic Stimulation and Motor Training Improves Functional Recovery and Perilesional Cortical Activity

Background. An ischemic stroke is followed by the remapping of motor representation and extensive changes in cortical excitability involving both hemispheres. Although stimulation of the ipsilesional motor cortex, especially when paired with motor training, facilitates plasticity and functional restoration, the remapping of motor representation of the single and combined treatments is largely unexplored. Objective. We investigated if spatio-temporal features of motor-related cortical activity and the new motor representations are related to the rehabilitative treatment or if they can be specifically associated to functional recovery. Methods. We designed a novel rehabilitative treatment that combines neuro-plasticizing intervention with motor training. In detail, optogenetic stimulation of peri-infarct excitatory neurons expressing Channelrhodopsin 2 was associated with daily motor training on a robotic device. The effectiveness of the combined therapy was compared with spontaneous recovery and with the single treatments (ie optogenetic stimulation or motor training). Results. We found that the extension and localization of the new motor representations are specific to the treatment, where most treatments promote segregation of the motor representation to the peri-infarct region. Interestingly, only the combined therapy promotes both the recovery of forelimb functionality and the rescue of spatio-temporal features of motor-related activity. Functional recovery results from a new excitatory/inhibitory balance between hemispheres as revealed by the augmented motor response flanked by the increased expression of parvalbumin positive neurons in the peri-infarct area. Conclusions. Our findings highlight that functional recovery and restoration of motor-related neuronal activity are not necessarily coupled during post-stroke recovery. Indeed the reestablishment of cortical activation features of calcium transient is distinctive of the most effective therapeutic approach, the combined therapy.

Intermanual transfer of visuomotor learning is facilitated by a cognitive strategy

Humans continuously adapt their movement to a novel environment by recalibrating their sensorimotor system. Recent evidence, however, shows that explicit planning to compensate for external changes, i.e. a cognitive strategy, can also aid performance. If such a strategy is indeed planned in external space, it should improve performance in an effector independent manner. We tested this hypothesis by examining whether promoting a cognitive strategy during a visual-force adaptation task performed in one hand can facilitate learning for the opposite hand. Participants rapidly adjusted the height of visual bar on screen to a target level by isometrically exerting force on a handle using their right hand. Visuomotor gain increased during the task and participants learned the increased gain. Visual feedback was continuously provided for one group, while for another group only the endpoint of the force trajectory was presented. The latter has been reported to promote cognitive strategy use. We found that endpoint feedback produced stronger intermanual transfer of learning and slower response times than continuous feedback. In a separate experiment, we confirmed that the aftereffect is indeed reduced when only endpoint feedback is provided, a finding that has been consistently observed when cognitive strategies are used. The results suggest that intermanual transfer can be facilitated by a cognitive strategy. This indicates that the behavioral observation of intermanual transfer can be achieved either by forming an effector-independent motor representation, or by sharing an effector-independent cognitive strategy between the hands.

Forearm and hand muscles exhibit high coactivation and overlapping of cortical motor representations

Most of the motor mapping procedures using navigated transcranial magnetic stimualiton (nTMS) follows the conventional somatotopic organization of the primary motor cortex (M1) by assessesing the representation of a particular target muscle, disregarding the possible coactivation of synergistic muscles. In turn, multiple reports describe a functional organization of the M1 with an overlapping among motor representations acting together to execute movements. In this context, the overlap degree among cortical representations of synergistic hand and forearm muscles remains an open question. This study aimed to evaluate the muscle coactivation and representation overlapping common to the grasping movement and its dependence on the mapping parameters. The nTMS motor maps were obtained from one carpal muscle and two intrinsic hand muscles during rest. We quantified the overlappig motor maps in terms of the size (area and volume overlap degree) and topography (similarity and centroid's Euclidian distance) parameters. We demonstrated that these muscle representations are highly overlapped and similar in shape. The overlap degrees involving the forearm muscles were significantly higher than only among the intrinsic hand muscles. Moreover, the stimulation intensity had a stronger effect on the size compared to the topography parameters. Our study contributes to a more detailed cortical motor representation towards a synergistic, functional arrangement of M1. Understanding the muscle group coactivation may provide more accurate motor maps when delineating the eloquent brain tissue during pre-surgical planning.

Large-scale all-optical dissection of motor cortex connectivity reveals a segregated functional organization of mouse forelimb representations

In rodent motor cortex, the rostral forelimb area (RFA) and the caudal forelimb area (CFA) are major actors in orchestrating the control of forelimb complex movements. However, their intrinsic connections and reciprocal functional organization are still unclear, limiting our understanding of how the brain coordinates and executes voluntary movements. Here we causally probed cortical connectivity and activation patterns triggered by transcranial optogenetic stimulation of ethologically relevant complex movements exploiting a novel large-scale all-optical method in awake mice. Results show specific activation features for each movement class, providing evidence for a segregated functional organization of CFA and RFA. Importantly, we identified a second discrete lateral grasping representation area, namely lateral forelimb area (LFA), with unique connectivity and activation patterns. Therefore, we propose the LFA as a distinct motor representation in the forelimb somatotopic motor map.

Common Brain Substrates Underlying Auditory Speech Priming and Perceived Spatial Separation

Under a “cocktail party” environment, listeners can utilize prior knowledge of the content and voice of the target speech [i.e., auditory speech priming (ASP)] and perceived spatial separation to improve recognition of the target speech among masking speech. Previous studies suggest that these two unmasking cues are not processed independently. However, it is unclear whether the unmasking effects of these two cues are supported by common neural bases. In the current study, we aimed to first confirm that ASP and perceived spatial separation contribute to the improvement of speech recognition interactively in a multitalker condition and further investigate whether there exist intersectant brain substrates underlying both unmasking effects, by introducing these two unmasking cues in a unified paradigm and using functional magnetic resonance imaging. The results showed that neural activations by the unmasking effects of ASP and perceived separation partly overlapped in brain areas: the left pars triangularis (TriIFG) and orbitalis of the inferior frontal gyrus, left inferior parietal lobule, left supramarginal gyrus, and bilateral putamen, all of which are involved in the sensorimotor integration and the speech production. The activations of the left TriIFG were correlated with behavioral improvements caused by ASP and perceived separation. Meanwhile, ASP and perceived separation also enhanced the functional connectivity between the left IFG and brain areas related to the suppression of distractive speech signals: the anterior cingulate cortex and the left middle frontal gyrus, respectively. Therefore, these findings suggest that the motor representation of speech is important for both the unmasking effects of ASP and perceived separation and highlight the critical role of the left IFG in these unmasking effects in “cocktail party” environments.

Effects of Unilateral Nasal Obstruction on the Development of the Cortical Masticatory Area in Growing Rats

The cortical masticatory area (CMA) regulates masticatory movements and controls rhythmic jaw movements. However, information regarding the effect of respiratory disturbances on the functional development of the CMA remains limited. This study aimed to examine the effect of chronic unilateral nasal obstruction (UNO) on the motor representation of the anterior digastric (AD) muscle during the growth period. Forty-eight 8-day-old male Wistar albino rats were randomized into control (CONT, n=24) and UNO (n=24) groups. Both groups underwent intracortical microstimulation (ICMS) at ages 5, 7, and 9 weeks. Arterial oxygen saturation (SpO2) and the number of positive ICMS sites for the AD muscle were measured throughout the experiment. The SpO2 values were significantly lower in the UNO group than in the CONT group at each age. Further, the number of positive ICMS sites for the AD muscle was significantly higher in the UNO group than in the CONT group at each age. Intragroup comparisons revealed that the number of positive ICMS sites increased with age. The onset latencies of the evoked AD potential significantly differed between the right and left sides. However, no differences were found between the CONT and UNO groups at any age. These findings suggest that UNO during development induces changes in the motor representation in the CMA.

Robotic hand augmentation drives changes in neural body representation

Humans have long been fascinated by the opportunities afforded through augmentation. This vision not only depends on technological innovations but also critically relies on our brain’s ability to learn, adapt, and interface with augmentation devices. Here, we investigated whether successful motor augmentation with an extra robotic thumb can be achieved and what its implications are on the neural representation and function of the biological hand. Able-bodied participants were trained to use an extra robotic thumb (called the Third Thumb) over 5 days, including both lab-based and unstructured daily use. We challenged participants to complete normally bimanual tasks using only the augmented hand and examined their ability to develop hand-robot interactions. Participants were tested on a variety of behavioral and brain imaging tests, designed to interrogate the augmented hand’s representation before and after the training. Training improved Third Thumb motor control, dexterity, and hand-robot coordination, even when cognitive load was increased or when vision was occluded. It also resulted in increased sense of embodiment over the Third Thumb. Consequently, augmentation influenced key aspects of hand representation and motor control. Third Thumb usage weakened natural kinematic synergies of the biological hand. Furthermore, brain decoding revealed a mild collapse of the augmented hand’s motor representation after training, even while the Third Thumb was not worn. Together, our findings demonstrate that motor augmentation can be readily achieved, with potential for flexible use, reduced cognitive reliance, and increased sense of embodiment. Yet, augmentation may incur changes to the biological hand representation. Such neurocognitive consequences are crucial for successful implementation of future augmentation technologies.