Motor Cost Influences Perceptual Decisions

Perceptual decision making has been widely studied using tasks in which subjects are asked to discriminate a visual stimulus and instructed to report their decision with a movement. In these studies, performance is measured by assessing the accuracy of the participants’ choices as a function of the ambiguity of the visual stimulus. Typically, the reporting movement is considered as a mere means of reporting the decision with no influence on the decision-making process. However, recent studies have shown that even subtle differences of biomechanical costs between movements may influence how we select between them. Here we investigated whether this purely motor cost could also influence decisions in a perceptual discrimination task in detriment of accuracy. In other words, are perceptual decisions only dependent on the visual stimulus and entirely orthogonal to motor costs? Here we show the results of a psychophysical experiment in which human subjects were presented with a random dot motion discrimination task and asked to report the perceived motion direction using movements of different biomechanical cost. We found that the pattern of decisions exhibited a significant bias towards the movement of lower cost, even when this bias reduced performance accuracy. This strongly suggests that motor costs influence decision making in visual discrimination tasks for which its contribution is neither instructed nor beneficial.     

Music Attenuates Excessive Visual Guidance of Skilled Reaching in Advanced but Not Mild Parkinson's Disease

Parkinson''s disease (PD) results in movement and sensory impairments that can be reduced by familiar music. At present, it is unclear whether the beneficial effects of music are limited to lessening the bradykinesia of whole body movement or whether beneficial effects also extend to skilled movements of PD subjects. This question was addressed in the present study in which control and PD subjects were given a skilled reaching task that was performed with and without accompanying preferred musical pieces. Eye movements and limb use were monitored with biomechanical measures and limb movements were additionally assessed using a previously described movement element scoring system. Preferred musical pieces did not lessen limb and hand movement impairments as assessed with either the biomechanical measures or movement element scoring. Nevertheless, the PD patients with more severe motor symptoms as assessed by Hoehn and Yahr (HY) scores displayed enhanced visual engagement of the target and this impairment was reduced during trials performed in association with accompanying preferred musical pieces. The results are discussed in relation to the idea that preferred musical pieces, although not generally beneficial in lessening skilled reaching impairments, may normalize the balance between visual and proprioceptive guidance of skilled reaching.     

Computational nature of human adaptive control during learning of reaching movements in force fields

Learning to make reaching movements in force fields was used as a paradigm to explore the system architecture of the biological adaptive controller. We compared the performance of a number of candidate control systems that acted on a model of the neuromuscular system of the human arm and asked how well the dynamics of the candidate system compared with the movement characteristics of 16 subjects. We found that control via a supra-spinal system that utilized an adaptive inverse model resulted in dynamics that were similar to that observed in our subjects, but lacked essential characteristics. These characteristics pointed to a different architecture where descending commands were influenced by an adaptive forward model. However, we found that control via a forward model alone also resulted in dynamics that did not match the behavior of the human arm. We considered a third control architecture where a forward model was used in conjunction with an inverse model and found that the resulting dynamics were remarkably similar to that observed in the experimental data. The essential property of this control architecture was that it predicted a complex pattern of near-discontinuities in hand trajectory in the novel force field. A nearly identical pattern was observed in our subjects, suggesting that generation of descending motor commands was likely through a control system architecture that included both adaptive forward and inverse models. We found that as subjects learned to make reaching movements, adaptation rates for the forward and inverse models could be independently estimated and the resulting changes in performance of subjects from movement to movement could be accurately accounted for. Results suggested that the adaptation of the forward model played a dominant role in the motor learning of subjects. After a period of consolidation, the rates of adaptation in the internal models were significantly larger than those observed before the memory had consolidated. This suggested that consolidation of motor memory coincided with freeing of certain computational resources for subsequent learning. Received: 01 January 1998 / Accepted in revised form: 26 January 1999     

Biomechanical aspects of gravitational training of the astronauts before the flight

Researchers tested a hypothesis that astronauts can become more proficient in training for tasks during space flight by training in a high gravity suit. Computer image analysis of movements, tensodynamography, and myotonometry were used to analyze movement in the hypergravity suit, muscle response, and other biomechanical factors. Results showed that training in the hypergravity suit improved the biomechanics of motor performance.     

Multiple Motor Learning Strategies in Visuomotor Rotation

Background

When exposed to a continuous directional discrepancy between movements of a visible hand cursor and the actual hand (visuomotor rotation), subjects adapt their reaching movements so that the cursor is brought to the target. Abrupt removal of the discrepancy after training induces reaching error in the direction opposite to the original discrepancy, which is called an aftereffect. Previous studies have shown that training with gradually increasing visuomotor rotation results in a larger aftereffect than with a suddenly increasing one. Although the aftereffect difference implies a difference in the learning process, it is still unclear whether the learned visuomotor transformations are qualitatively different between the training conditions.

Methodology/Principal Findings

We examined the qualitative changes in the visuomotor transformation after the learning of the sudden and gradual visuomotor rotations. The learning of the sudden rotation led to a significant increase of the reaction time for arm movement initiation and then the reaching error decreased, indicating that the learning is associated with an increase of computational load in motor preparation (planning). In contrast, the learning of the gradual rotation did not change the reaction time but resulted in an increase of the gain of feedback control, suggesting that the online adjustment of the reaching contributes to the learning of the gradual rotation. When the online cursor feedback was eliminated during the learning of the gradual rotation, the reaction time increased, indicating that additional computations are involved in the learning of the gradual rotation.

Conclusions/Significance

The results suggest that the change in the motor planning and online feedback adjustment of the movement are involved in the learning of the visuomotor rotation. The contributions of those computations to the learning are flexibly modulated according to the visual environment. Such multiple learning strategies would be required for reaching adaptation within a short training period.     

Measuring generalization of visuomotor perturbations in wrist movements using mobile phones

Recent studies in motor control have shown that visuomotor rotations for reaching have narrow generalization functions: what we learn during movements in one direction only affects subsequent movements into close directions. Here we wanted to measure the generalization functions for wrist movement. To do so we had 7 subjects performing an experiment holding a mobile phone in their dominant hand. The mobile phone's built in acceleration sensor provided a convenient way to measure wrist movements and to run the behavioral protocol. Subjects moved a cursor on the screen by tilting the phone. Movements on the screen toward the training target were rotated and we then measured how learning of the rotation in the training direction affected subsequent movements in other directions. We find that generalization is local and similar to generalization patterns of visuomotor rotation for reaching.     

Nonvisual motor training influences biological motion perception

Experimental evidence suggests a link between perception and the execution of actions . In particular, it has been proposed that motor programs might directly influence visual action perception . According to this hypothesis, the acquisition of novel motor behaviors should improve their visual recognition, even in the absence of visual learning. We tested this prediction by using a new experimental paradigm that dissociates visual and motor learning during the acquisition of novel motor patterns. The visual recognition of gait patterns from point-light stimuli was assessed before and after nonvisual motor training. During this training, subjects were blindfolded and learned a novel coordinated upper-body movement based only on verbal and haptic feedback. The learned movement matched one of the visual test patterns. Despite the absence of visual stimulation during training, we observed a selective improvement of the visual recognition performance for the learned movement. Furthermore, visual recognition performance after training correlated strongly with the accuracy of the execution of the learned motor pattern. These results prove, for the first time, that motor learning has a direct and highly selective influence on visual action recognition that is not mediated by visual learning.     

Reinforcement Learning of Targeted Movement in a Spiking Neuronal Model of Motor Cortex

Sensorimotor control has traditionally been considered from a control theory perspective, without relation to neurobiology. In contrast, here we utilized a spiking-neuron model of motor cortex and trained it to perform a simple movement task, which consisted of rotating a single-joint “forearm” to a target. Learning was based on a reinforcement mechanism analogous to that of the dopamine system. This provided a global reward or punishment signal in response to decreasing or increasing distance from hand to target, respectively. Output was partially driven by Poisson motor babbling, creating stochastic movements that could then be shaped by learning. The virtual forearm consisted of a single segment rotated around an elbow joint, controlled by flexor and extensor muscles. The model consisted of 144 excitatory and 64 inhibitory event-based neurons, each with AMPA, NMDA, and GABA synapses. Proprioceptive cell input to this model encoded the 2 muscle lengths. Plasticity was only enabled in feedforward connections between input and output excitatory units, using spike-timing-dependent eligibility traces for synaptic credit or blame assignment. Learning resulted from a global 3-valued signal: reward (+1), no learning (0), or punishment (−1), corresponding to phasic increases, lack of change, or phasic decreases of dopaminergic cell firing, respectively. Successful learning only occurred when both reward and punishment were enabled. In this case, 5 target angles were learned successfully within 180 s of simulation time, with a median error of 8 degrees. Motor babbling allowed exploratory learning, but decreased the stability of the learned behavior, since the hand continued moving after reaching the target. Our model demonstrated that a global reinforcement signal, coupled with eligibility traces for synaptic plasticity, can train a spiking sensorimotor network to perform goal-directed motor behavior.     

Neural basis of learning new movements: evolution of classical concepts

According to classical consepts, the role of the motor cortex in performance of skilled movements of distal parts of extremities is confined to control of appropriate motoneurons by the "point-to-point" principle. However, much evidence of plasticity of the motor cortex and its active role in motor learning appeared in last decade. Fos-gene expression in the motor cortex was found to accompany learning a skill. Strengthening of horizontal pathways in layers II-III was revealed, and cholinergic input to tese layers was found to be important. The imaging data show that activity of the motor cortex increases during motor practice as well. This raises the question of specificity of the motor cortex in the motor learning per se. During acquisition of new movements some previously used synergies prevent the necessary coordination from being learned, so they must be suppressed in the process of motor learning. Investigations of central mechanisms of coordination interference in humans are still at the beginning. However, there are some animal models of reorganization and suppression of interfering synergies. The reorganization and suppression of coordination preventing realization of a new movement is shown to be a specific function of the motor cortex. After automation of new synergies the cortical control is still present, as distinct from the learned movements, which do not require suppression of interfering synergies. However, it does not mean that the conscious control of the performance is still present.     

Two Agents in the Brain: Motor Control of Unimanual and Bimanual Reaching Movements

Previous studies have suggested that the left and right hands have different specialties for motor control that can be represented as two agents in the brain. This study examined how coordinated movements are performed during bimanual reaching tasks to highlight differences in the characteristics of the hands. We examined motor movement accuracy, reaction time, and movement time in right-handed subjects performing a three-dimensional motor control task (visually guided reaching). In the no-visual-feedback condition, right-hand movement had lower accuracy and a shorter reaction time than did left-hand movement, whereas bimanual movement had the longest reaction time, but the best accuracy. This suggests that the two hands have different internal models and specialties: closed-loop control for the right hand and open-loop control for the left hand. Consequently, during bimanual movements, both models might be used, creating better control and planning (or prediction), but requiring more computation time compared to the use of one hand only.     

Interference in ballistic motor learning: specificity and role of sensory error signals

Humans are capable of learning numerous motor skills, but newly acquired skills may be abolished by subsequent learning. Here we ask what factors determine whether interference occurs in motor learning. We speculated that interference requires competing processes of synaptic plasticity in overlapping circuits and predicted specificity. To test this, subjects learned a ballistic motor task. Interference was observed following subsequent learning of an accuracy-tracking task, but only if the competing task involved the same muscles and movement direction. Interference was not observed from a non-learning task suggesting that interference requires competing learning. Subsequent learning of the competing task 4 h after initial learning did not cause interference suggesting disruption of early motor memory consolidation as one possible mechanism underlying interference. Repeated transcranial magnetic stimulation (rTMS) of corticospinal motor output at intensities below movement threshold did not cause interference, whereas suprathreshold rTMS evoking motor responses and (re)afferent activation did. Finally, the experiments revealed that suprathreshold repetitive electrical stimulation of the agonist (but not antagonist) peripheral nerve caused interference. The present study is, to our knowledge, the first to demonstrate that peripheral nerve stimulation may cause interference. The finding underscores the importance of sensory feedback as error signals in motor learning. We conclude that interference requires competing plasticity in overlapping circuits. Interference is remarkably specific for circuits involved in a specific movement and it may relate to sensory error signals.     

Arm-plane representation of shoulder compensation during pointing movements in patients with stroke

Improvements in functional motor activities are often accompanied by motor compensations to overcome persistent motor impairment in the upper limb. Kinematic analysis is used to objectively quantify movement patterns including common motor compensations such as excessive trunk displacement during reaching. However, a common motor compensation to assist reaching, shoulder abduction, is not adequately characterized by current motion analysis approaches. We apply the arm-plane representation that accounts for the co-variation between movements of the whole arm, and investigate its ability to identify and quantify compensatory arm movements in stroke subjects when making forward arm reaches. This method has not been previously applied to the analysis of motion deficits. Sixteen adults with right post-stroke hemiparesis and eight healthy age-matched controls reached in three target directions (14 trials/target; sampling rate: 100 Hz). Arm-plane movement was validated against endpoint, joint, and trunk kinematics and compared between groups. In stroke subjects, arm-plane measures were correlated with arm impairment (Fugl-Meyer Assessment) and ability (Box and Blocks) scores and were more sensitive than clinical measures to detect mild motor impairment. Arm-plane motion analysis provides new information about motor compensations involving the co-variation of shoulder and elbow movements that may help to understand the underlying motor deficits in patients with stroke.     

Computational model of motor learning and perceptual change

Motor learning in the context of arm reaching movements has been frequently investigated using the paradigm of force-field learning. It has been recently shown that changes to somatosensory perception are likewise associated with motor learning. Changes in perceptual function may be the reason that when the perturbation is removed following motor learning, the hand trajectory does not return to a straight line path even after several dozen trials. To explain the computational mechanisms that produce these characteristics, we propose a motor control and learning scheme using a simplified two-link system in the horizontal plane: We represent learning as the adjustment of desired joint-angular trajectories so as to achieve the reference trajectory of the hand. The convergence of the actual hand movement to the reference trajectory is proved by using a Lyapunov-like lemma, and the result is confirmed using computer simulations. The model assumes that changes in the desired hand trajectory influence the perception of hand position and this in turn affects movement control. Our computer simulations support the idea that perceptual change may come as a result of adjustments to movement planning with motor learning.     

Eye-Hand Coordination during Visuomotor Adaptation with Different Rotation Angles: Effects of Terminal Visual Feedback

This study examined adaptive changes of eye-hand coordination during a visuomotor rotation task under the use of terminal visual feedback. Young adults made reaching movements to targets on a digitizer while looking at targets on a monitor where the rotated feedback (a cursor) of hand movements appeared after each movement. Three rotation angles (30°, 75° and 150°) were examined in three groups in order to vary the task difficulty. The results showed that the 30° group gradually reduced direction errors of reaching with practice and adapted well to the visuomotor rotation. The 75° group made large direction errors of reaching, and the 150° group applied a 180° reversal shift from early practice. The 75°and 150° groups, however, overcompensated the respective rotations at the end of practice. Despite these group differences in adaptive changes of reaching, all groups gradually adapted gaze directions prior to reaching from the target area to the areas related to the final positions of reaching during the course of practice. The adaptive changes of both hand and eye movements in all groups mainly reflected adjustments of movement directions based on explicit knowledge of the applied rotation acquired through practice. Only the 30° group showed small implicit adaptation in both effectors. The results suggest that by adapting gaze directions from the target to the final position of reaching based on explicit knowledge of the visuomotor rotation, the oculomotor system supports the limb-motor system to make precise preplanned adjustments of reaching directions during learning of visuomotor rotation under terminal visual feedback.     

European Society of Biomechanics S.M. Perren Award 2018: Altered biomechanical stimulation of the developing hip joint in presence of hip dysplasia risk factors

Fetal kicking and movements generate biomechanical stimulation in the fetal skeleton, which is important for prenatal musculoskeletal development, particularly joint shape. Developmental dysplasia of the hip (DDH) is the most common joint shape abnormality at birth, with many risk factors for the condition being associated with restricted fetal movement. In this study, we investigate the biomechanics of fetal movements in such situations, namely fetal breech position, oligohydramnios and primiparity (firstborn pregnancy). We also investigate twin pregnancies, which are not at greater risk of DDH incidence, despite the more restricted intra-uterine environment. We track fetal movements for each of these situations using cine-MRI technology, quantify the kick and muscle forces, and characterise the resulting stress and strain in the hip joint, testing the hypothesis that altered biomechanical stimuli may explain the link between certain intra-uterine conditions and risk of DDH. Kick force, stress and strain were found to be significantly lower in cases of breech position and oligohydramnios. Similarly, firstborn fetuses were found to generate significantly lower kick forces than non-firstborns. Interestingly, no significant difference was observed in twins compared to singletons. This research represents the first evidence of a link between the biomechanics of fetal movements and the risk of DDH, potentially informing the development of future preventative measures and enhanced diagnosis. Our results emphasise the importance of ultrasound screening for breech position and oligohydramnios, particularly later in pregnancy, and suggest that earlier intervention to correct breech position through external cephalic version could reduce the risk of hip dysplasia.     

Striatal level of regulation of learned forepaw movements in rats

The role of the striatal adenylyl cyclase (AC) and cholinergic systems in the learning and expression of new forepaw movements (reaching with prolonged pushing on a fixed piston) was studied in male Wistar rats. Motor learning processes, prenatal hypoxia, and cholinergic drugs changed the properties of the AC system in the striatum. After learning, the striatal basal AC activity was decreased compared to untrained control rats. In addition, the AC activity was more decreased in animals with a good ability to learn compared to poor learners (up to 31 % and 51 %, correspondingly; p<0.01). Rats subjected to prenatal hypoxia (13-14th days of embryogenesis) had a lower ability to learn the new movements requiring tactile control and the striatal AC activity in these rats was 1.8 times higher (p<0.001) than controls. In vitro application of the cholinergic agonist carbachol (CARB) 10-5 M (corresponding to approximately 0.3 microg), as well as the antagonist scopolomine (SCOP) 10(-5) M (approximately 0.3 microg) decreased AC activity in the synaptosomal fraction of the striatum. In vivo injections of CARB (0.3-3 microg/1microl) or SCOP (0.3-3 microg/1microl) into the ventral striatum (nucleus accumbens) modified the newly learned sensorimotor skill. After CARB injections the rats performed slower movements with more prolonged pushing. After SCOP the rats could not retain the learned pushing movement. These in vivo and in vitro data suggest that the cholinergic mediator system of the striatum is involved in learning sensory-controlled forepaw movements as well as the regulation of new motor skills by modulating the AC signal transduction process in the striatum. The data confirmed that modification of the striatal AC system resulted in the modulation of reaching behavior and better expression of the learned reflex.     

Attention modulation regulates both motor and non-motor performance: a high-density EEG study in Parkinson's disease

We have previously shown that, in early stages of Parkinson's disease (PD), patients with higher reaction times are also more impaired in visual sequence learning, suggesting that movement preparation shares resources with the learning of visuospatial sequences. Here, we ascertained whether, in patients with PD, the pattern of the neural correlates of attentional processes of movement planning predict sequence learning and working memory abilities. High density Electroencephalography (EEG, 256 electrodes) was recorded in 19 patients with PD performing reaching movements in a choice reaction time paradigm. Patients were also tested with Digit Span and performed a visuomotor sequence learning task that has an important declarative learning component. We found that attenuation of alpha/beta oscillatory activity before the stimulus presentation in frontoparietal regions significantly correlated with reaction time in the choice reaction time task, similarly to what we had previously found in normal subjects. In addition, such activity significantly predicted the declarative indices of sequence learning and the scores in the Digit Span task. These findings suggest that some motor and non motor PD signs might have common neural bases, and thus, might have a similar response to the same behavioral therapy. In addition, these results might help in designing and testing the efficacy of novel rehabilitative approaches to improve specific aspects of motor performance in PD and other neurological disorders.     

Sleep-Dependent Reactivation of Ensembles in Motor Cortex Promotes Skill Consolidation

Despite many prior studies demonstrating offline behavioral gains in motor skills after sleep, the underlying neural mechanisms remain poorly understood. To investigate the neurophysiological basis for offline gains, we performed single-unit recordings in motor cortex as rats learned a skilled upper-limb task. We found that sleep improved movement speed with preservation of accuracy. These offline improvements were linked to both replay of task-related ensembles during non-rapid eye movement (NREM) sleep and temporal shifts that more tightly bound motor cortical ensembles to movements; such offline gains and temporal shifts were not evident with sleep restriction. Interestingly, replay was linked to the coincidence of slow-wave events and bursts of spindle activity. Neurons that experienced the most consistent replay also underwent the most significant temporal shift and binding to the motor task. Significantly, replay and the associated performance gains after sleep only occurred when animals first learned the skill; continued practice during later stages of learning (i.e., after motor kinematics had stabilized) did not show evidence of replay. Our results highlight how replay of synchronous neural activity during sleep mediates large-scale neural plasticity and stabilizes kinematics during early motor learning.     

Visual feedback is not necessary for the learning of novel dynamics

Background

When learning to perform a novel sensorimotor task, humans integrate multi-modal sensory feedback such as vision and proprioception in order to make the appropriate adjustments to successfully complete the task. Sensory feedback is used both during movement to control and correct the current movement, and to update the feed-forward motor command for subsequent movements. Previous work has shown that adaptation to stable dynamics is possible without visual feedback. However, it is not clear to what degree visual information during movement contributes to this learning or whether it is essential to the development of an internal model or impedance controller.

Methodology/Principle Findings

We examined the effects of the removal of visual feedback during movement on the learning of both stable and unstable dynamics in comparison with the case when both vision and proprioception are available. Subjects were able to learn to make smooth movements in both types of novel dynamics after learning with or without visual feedback. By examining the endpoint stiffness and force after learning it could be shown that subjects adapted to both types of dynamics in the same way whether they were provided with visual feedback of their trajectory or not. The main effects of visual feedback were to increase the success rate of movements, slightly straighten the path, and significantly reduce variability near the end of the movement.

Conclusions/Significance

These findings suggest that visual feedback of the hand during movement is not necessary for the adaptation to either stable or unstable novel dynamics. Instead vision appears to be used to fine-tune corrections of hand trajectory at the end of reaching movements.