Artificial gravity as a countermeasure in long-duration space flight

Long-duration exposure to weightlessness results in bone demineralization, muscle atrophy, cardiovascular deconditioning, altered sensory-motor control, and central nervous system reorganizations. Exercise countermeasures and body loading methods so far employed have failed to prevent these changes. A human mission to Mars might last 2 or 3 years and without effective countermeasures could result in dangerous levels of bone and muscle loss. Artificial gravity generated by rotation of an entire space vehicle or of an inner chamber could be used to prevent structural changes. Some of the physical characteristics of rotating environments are outlined along with their implications for human performance. Artificial gravity is the centripetal force generated in a rotating vehicle and is proportional to the product of the square of angular velocity and the radius of rotation. Thus, for a particular g-level, there is a tradeoff between velocity of rotation and radius. Increased radius is vastly more expensive to achieve than velocity, so it is important to know the highest rotation rates to which humans can adapt. Early studies suggested that 3 rpm might be the upper limit because movement control and orientation were disrupted at higher velocities and motion sickness and chronic fatigue were persistent problems. Recent studies, however, are showing that, if the terminal velocity is achieved over a series of gradual steps and many body movements are made at each dwell velocity, then full adaptation of head, arm, and leg movements is possible. Rotation rates as high as 7.5-10 rpm are likely feasible. An important feature of the new studies is that they provide compelling evidence that equilibrium point theories of movement control are inadequate. The central principles of equilibrium point theories lead to the equifinality prediction, which is violated by movements made in rotating reference frames.     

Prediction of the body rotation-induced torques on the arm during reaching movements: evidence from a proprioceptively deafferented subject

Reaching for a target while rotating the trunk generates substantial Coriolis and centrifugal torques that push the arm in the opposite direction of the rotations. These torques rarely perturb movement accuracy, suggesting that they are compensated for during the movement. Here we tested whether signals generated during body motion (e.g., vestibular) can be used to predict the torques induced by the body rotation and to modify the motor commands accordingly. We asked a deafferented subject to reach for a memorized visual target in darkness. At the onset of the reaching, the patient was rotated 25° or 40° in the clockwise or the counterclockwise directions. During the rotation, the patient's head remained either fixed in space (Head-Fixed condition) or fixed on the trunk (Head Rotation condition). At the rotation onset, the deafferented patient's hand largely deviated from the mid-sagittal plane in both conditions. The hand deviations were compensated for in the Head Rotation condition only. These results highlight the computational faculty of the brain and show that body rotation-related information can be processed for predicting the consequence of the rotation dynamics on the reaching arm movements.     

Compensatory arm–trunk coordination in pointing movements is preserved in the absence of visual feedback

This study examined the influence of trunk recruitment on the kinematic characteristics of pointing movements. The distribution of final positions of the hand, the extent and direction of the hand trajectory was basically preserved when trunk movement was combined with arm pointing. These effects were observed during pointing not only with but also without vision. The results imply that two functionally independent units of coordination are used in pointing regardless of visual feedback-one producing arm movement to the target (the reaching synergy) and the other coordinating trunk and arm movements diminishing the influence of the trunk on the arm endpoint trajectory (the compensatory synergy).     

Pushing attention to one side: Force field adaptation alters neural correlates of orienting and disengagement of spatial attention

Sensorimotor adaptation to wedge prisms can alter the balance of attention between left and right space in healthy adults, and improve symptoms of spatial neglect after stroke. Here we asked whether the orienting of spatial attention to visual stimuli is affected by a different form of sensorimotor adaptation that involves physical perturbations of arm movement, rather than distortion of visual feedback. Healthy participants performed a cued discrimination task before and after they made reaching movements to a central target. A velocity‐dependent force field pushed the hand aside during each reach, and required participants to apply compensatory forces toward the opposite side. We used event‐related potentials (ERPs) to determine whether electroencephalography (EEG) responses reflecting orienting (cue‐locked N1) and disengagement (target‐locked P1) of spatial attention are affected by adaptation to force fields. After adaptation, the cue‐locked N1 was relatively larger for stimuli presented in the hemispace corresponding to the direction of compensatory hand force. P1 amplitudes evoked by invalidly cued targets presented on the opposite side were reduced. This suggests that force field adaptation boosted attentional orienting responses toward the side of hand forces, and impeded attentional disengagement from that side, mimicking previously reported effects of prism adaptation. Thus, remapping between motor commands and intended movement direction is sufficient to bias ERPs, reflecting changes in the orienting of spatial attention in the absence of visuo‐spatial distortion or visuo‐proprioceptive mismatch. Findings are relevant to theories of how sensorimotor adaptation can modulate attention, and may open new avenues for treatment of spatial neglect.     

Abnormal sensorimotor control, but intact force field adaptation, in multiple sclerosis subjects with no clinical disability

In MS subjects with no clinical disability, we assessed sensorimotor organization and their ability to adapt to an unfamiliar dynamical environment. Eleven MS subjects performed reaching movements while a robot generated a speed-dependent force field. Control and adaptation performance were compared with that of an equal number of control subjects. During a familiarization phase, when the robot generated no forces, the movements of MS subjects were more curved, displayed greater and more variable directional errors and a longer deceleration phase. During the force field phase, both MS and control subjects gradually learned to predict the robot-generated forces. The rates of adaptation were similar, but MS subjects showed a greater variability in responding to the force field. These results suggest that MS subjects have a preserved capability of learning to predict the effects of the forces, but make greater errors when actually using such predictions to generate movements. Inaccurate motor commands are then compensated later in the movement through an extra amount of sensory-based corrections. This indicates that early in the disease MS subjects have intact adaptive capabilities, but impaired movement execution.     

Differential Effects of Cerebellar Degeneration on Feedforward versus Feedback Control across Speech and Reaching Movements

Errors that result from a mismatch between predicted movement outcomes and sensory afference are used to correct ongoing movements through feedback control and to adapt feedforward control of future movements. The cerebellum has been identified as a critical part of the neural circuit underlying implicit adaptation across a wide variety of movements (reaching, gait, eye movements, and speech). The contribution of this structure to feedback control is less well understood. Although it has recently been shown in the speech domain that individuals with cerebellar degeneration produce larger online corrections for sensory perturbations than control participants, similar behavior has not been observed in other motor domains. Currently, comparisons across domains are limited by different population samples and potential ceiling effects in existing tasks. To assess the relationship between changes in feedforward and feedback control associated with cerebellar degeneration across motor domains, we evaluated adaptive (feedforward) and compensatory (feedback) responses to sensory perturbations in reaching and speech production in human participants of both sexes with cerebellar degeneration and neurobiologically healthy controls. As expected, the cerebellar group demonstrated impaired adaptation in both reaching and speech. In contrast, the groups did not differ in their compensatory response in either domain. Moreover, compensatory and adaptive responses in the cerebellar group were not correlated within or across motor domains. These results point to a general impairment in feedforward control with spared feedback control in cerebellar degeneration. However, the magnitude of feedforward impairments and potential changes in feedback-based control manifest in a domain-specific manner across individuals.SIGNIFICANCE STATEMENT The cerebellum contributes to feedforward updating of movement in response to sensory errors, but its role in feedback control is less understood. Here, we tested individuals with cerebellar degeneration (CD), using sensory perturbations to assess adaptation of feedforward control and feedback gains during reaching and speech production tasks. The results confirmed that CD leads to reduced adaption in both domains. However, feedback gains were unaffected by CD in either domain. Interestingly, measures of feedforward and feedback control were not correlated across individuals within or across motor domains. Together, these results indicate a general impairment in feedforward control with spared feedback control in CD. However, the magnitude of feedforward impairments manifests in a domain-specific manner across individuals.     

Vision of the hand prior to movement onset allows full motor adaptation to a multi-force environment

In everyday life, because of unexpected mechanical perturbation applied to the hand or to the whole body, hand movements may become suddenly inaccurate. With prolonged exposure to the perturbation, trajectories slowly recover their normal accuracy, which is the mark of motor adaptation. However, full development of this adaptive process in complete darkness has been recently challenged in a multi-force environment. Here, we report on the effectiveness of static hand position information as specified through vision prior to movement onset on the adaptative changes, over trials, of pointing movements performed in a gravitoinertial force field. For this, subjects seated off-center on a platform rotating at constant velocity, were either confined to complete darkness (No Vision Session, NV) or provided with vision of the hand resting on the starting position prior to movement onset (Hand Vision Prior to Movement Session, HVPM). Overall, our results showed that adaptation to the centrifugal force was very rapid, and allowed subjects to demonstrate appropriate motor control as early as of the very first trials performed during the rotation period, even in the NV condition. They also showed that the integration by the Central Nervous System (CNS) of visual and proprioceptive information prior to the execution of a reaching movement allows subjects to reach full motor adaptation in a multi-force environment. Furthermore, our data confirm the existence of differentiated motor adaptive mechanisms for centrifugal and Coriolis forces. Adaptation to the former may fully develop on the basis of an a priori coding of the characteristics of the background force level even without visual information, while the latter needs visual cues about hand position prior to movement onset to take place.     

Intermittent visual feedback can boost motor learning of rhythmic movements: evidence for error feedback beyond cycles

Movement error is a driving force behind motor learning. For motor learning with discrete movements, such as point-to-point reaching, it is believed that the brain uses error information of the immediately preceding movement only. However, in the case of continuous and repetitive movements (i.e., rhythmic movements), there is a ceaseless inflow of performance information. Thus, an accurate temporal association of the motor commands with the resultant movement errors is not necessarily guaranteed. We investigated how the brain overcomes this challenging situation. Human participants adapted rhythmic movements between two targets to visuomotor rotations, the amplitudes of which changed randomly from cycle to cycle (the duration of one cycle was ～400 ms). A system identification technique revealed that the motor adaptation was affected not just by the preceding movement error, but also by a history of errors from the previous cycles. Error information obtained from more than one previous cycle tended to increase, rather than decrease, movement error. This result led to a counterintuitive prediction: providing visual error feedback for only a fraction of cycles should enhance visuomotor adaptation. As predicted, we observed that motor adaptation to a constant visual rotation (30°) was significantly enhanced by providing visual feedback once every fourth or fifth cycle rather than for every cycle. These results suggest that the brain requires a specific processing time to modify the motor command, based on the error information, and so is unable to deal appropriately with the overwhelming flow of error information generated during rhythmic movements.     

Gain field encoding of the kinematics of both arms in the internal model enables flexible bimanual action

Bimanual action requires the neural controller (internal model) for each arm to predictively compensate for mechanical interactions resulting from movement of both that arm and its counterpart on the opposite side of the body. Here, we demonstrate that the brain may accomplish this by constructing the internal model with primitives multiplicatively encoding information from the kinematics of both arms. We had human participants adapt to a novel force field imposed on one arm while both arms were moving in particular directions and examined the generalization pattern of motor learning when changing the movement directions of both arms. The generalization pattern was consistent with the pattern predicted from the multiplicative encoding scheme. As proposed by previous theoretical studies, the strength of multiplicative encoding was manifested in the observation that participants could adapt reaching movements to complicated force fields depending nonlinearly on the movement directions of both arms. These results indicate that multiplicative neuronal influence of the kinematics of the opposing arm on the internal models enables the brain to control bimanual movement by providing great flexible ability to handle arbitrary dynamical environments resulting from the interactions of both arms.     

Developmental lesions of visual cortex influence control of reaching

We examined visually guided reaching movements in a young adult (EW) who had extensive bilateral lesions in the visual cortex since birth. EW lacked a right occipital lobe and ventral portions of the left and had poor visual acuity (3/400), yet could point to visual targets as quickly as 9 controls with visual cortex lesions acquired in adulthood and 4 adults without neurological disease. However, EW's endpoint variability and hand movement path curvature were much greater, especially for left hand movements, in concert with large sensorimotor transformation errors. Experimental reduction of acuity (to 3/240 or worse) in the normal controls produced symmetric increases in endpoint variability but did not change hand path curvature, indicating that EW's impaired movements were not due to poor vision alone. Results suggest that visual cortex in early life supports the development of lifelong neural mechanisms for the planning and control of reaching movements.     

Role of the cerebellum in reaching movements in humans. I. Distributed inverse dynamics control

This study focuses on the role of the motor cortex, the spinal cord and the cerebellum in the dynamics stage of the control of arm movement. Currently, two classes of models have been proposed for the neural control of movements, namely the virtual trajectory control hypothesis and the acquisition of internal models of the motor apparatus hypothesis. In the present study, we expand the virtual trajectory model to whole arm reaching movements. This expanded model accurately reproduced slow movements, but faster reaching movements deviated significantly from the planned trajectories, indicating that for fast movements, this model was not sufficient. These results led us to propose a new distributed functional model consistent with behavioural, anatomical and neurophysiological data, which takes into account arm muscles, spinal cord, motor cortex and cerebellum and is consistent with the view that the central nervous system acquires a distributed inverse dynamics model of the arm. Previous studies indicated that the cerebellum compensates for the interaction forces that arise during reaching movements. We show here how the cerebellum may increase the accuracy of reaching movements by compensating for the interaction torques by learning a portion of an inverse dynamics model that refines a basic inverse model in the motor cortex and spinal cord.     

Arm trajectories in dyskinetic cerebral palsy have increased random variability

Dyskinetic cerebral palsy results from injury to the basal ganglia early in life. Symptoms can include hyperkinetic or dystonic arm movements that impair function. It is not known whether these movements comprise a small number of specific abnormal motor patterns or whether they are random and variable. We hypothesize that injury to the basal ganglia leads to impaired filtering and removal of undesired neural signals and that lack of appropriate removal of noisy or irrelevant neural signals leads to random and variable arm movements. To test this hypothesis, we quantified the variability in arm trajectories while seven children with dyskinetic cerebral palsy between the ages of 4 and 13 years old made repeated outward reaching movements. We compared the results with those of 21 healthy children between the ages of 5 and 16 years. The best-fit trajectory to the set of reaching movements for each child was taken as the predictable component of movement. We calculated the ratio of the power in the best-fit trajectory to the total variance. This measure is the signal-to-noise ratio, and it quantifies the extent to which trajectories are predictable. We found that children with dyskinetic cerebral palsy had a significantly reduced signal-to-noise ratio compared with healthy children at similar ages. This result shows that there is increased movement variability, and it is consistent with the hypothesis that inadequate removal of noisy signals could be a cause of the movement disorder in dyskinetic cerebral palsy.     

Feedback and feedforward adaptation to visuomotor delay during reaching and slicing movements

It has been suggested that the brain and in particular the cerebellum and motor cortex adapt to represent the environment during reaching movements under various visuomotor perturbations. It is well known that significant delay is present in neural conductance and processing; however, the possible representation of delay and adaptation to delayed visual feedback has been largely overlooked. Here we investigated the control of reaching movements in human subjects during an imposed visuomotor delay in a virtual reality environment. In the first experiment, when visual feedback was unexpectedly delayed, the hand movement overshot the end‐point target, indicating a vision‐based feedback control. Over the ensuing trials, movements gradually adapted and became accurate. When the delay was removed unexpectedly, movements systematically undershot the target, demonstrating that adaptation occurred within the vision‐based feedback control mechanism. In a second experiment designed to broaden our understanding of the underlying mechanisms, we revealed similar after‐effects for rhythmic reversal (out‐and‐back) movements. We present a computational model accounting for these results based on two adapted forward models, each tuned for a specific modality delay (proprioception or vision), and a third feedforward controller. The computational model, along with the experimental results, refutes delay representation in a pure forward vision‐based predictor and suggests that adaptation occurred in the forward vision‐based predictor, and concurrently in the state‐based feedforward controller. Understanding how the brain compensates for conductance and processing delays is essential for understanding certain impairments concerning these neural delays as well as for the development of brain–machine interfaces.     

Protection and expression of human motor memories

When we adapt our movements to a perturbation, and then adapt to another perturbation, is the initial memory destroyed, or is it protected? Despite decades of experiments, this question remains unresolved. The confusion, in our view, is due to the fact that in every instance the approach has been to assay contents of motor memory by retesting with the same perturbations. When performance in retesting is the same as naive, this is usually interpreted as the memory being destroyed. However, it is also possible that the initial memory is simply masked by the competing memory. We trained humans in a reaching task in field B and then in field A (or washout) over an equal number of trials. To assay contents of motor memory, we used a new tool: after completion of training in A, we withheld reinforcement (i.e., reward) for a brief block of trials and then clamped movement errors to zero over a long block of trials. We found that this led to spontaneous recovery of B. That is, withholding reinforcement for the current motor output resulted in the expression of the competing memory. Therefore, adaptation followed by washout or reverse adaptation produced competing motor memories. The protection from unlearning was unrelated to sudden changes in performance errors that might signal a contextual change, as competing memories formed even when the perturbations were introduced gradually. Rather, reinforcement appears to be a critical signal that affords protection to motor memories, and lack of reinforcement encourages retrieval of a competing memory.     

Skilled forelimb reaching for pasta guided by tactile input in the rat as measured by accuracy, spatial adjustments, and force

Rats are capable of reaching for food with a single forelimb, but since they locate the target of their reach using olfaction, it is unclear how they adjust their limb movement to compensate for errors. Although it is thought that their reaching movement is ballistic and can only be adjusted by trial and error, whether they can use haptic cues to aid in locating and identifying a target has not been examined. The present study addressed this question by allowing rats to reach through a slot for rigidly held pieces of uncooked pasta of varying thickness, which could be oriented vertically or horizontally from different points around the slot and which were attached to a force transducer. The tasks required that animals not only adjust their reach and grasp to the target's location but also identify the target based on its texture. Acquisition curves were made of head orientation, limb transport trajectories, number of attempts per success, paw orientation, breaking direction and force of the grasp. A haptic discrimination test used pasta and similar sized metal rods with different tactile properties as discriminanda. The results indicated that whereas postural orientation and limb transport trajectory were not modified as a function of target orientation, paw orientation and grasp force did vary as a function of the sensory qualities of the target object, and the rats could make a haptic discriminative choice of a target object. The results show that the rat is capable of adjusting paw movements using haptic information, suggesting that somatosensory features of sensorimotor control of limb and paw movements in carnivores and primates are shared by rodents. This commonality points to a conservation of motor control in mammals, explains some of the idiosyncratic features of rat reaching behavior, and confirms that rodents provide a good model for investigating sensorimotor functions.     

Visuomotor transformations underlying arm movements toward visual targets: a neural network model of cerebral cortical operations.

We propose a biologically realistic neural network that computes coordinate transformations for the command of arm reaching movements in 3-D space. This model is consistent with anatomical and physiological data on the cortical areas involved in the command of these movements. Studies of the neuronal activity in the motor (Georgopoulos et al., 1986; Schwartz et al., 1988; Caminiti et al., 1990a) and premotor (Caminiti et al., 1990b, 1991) cortices of behaving monkeys have shown that the activity of individual arm-related neurons is broadly tuned around a preferred direction of movements in 3-D space. Recent data demonstrate that in both frontal areas (Caminiti et al., 1990a,b, 1991) these cell preferred directions rotate with the initial position of the arm. Furthermore, the rotation of the population of preferred directions precisely corresponds to the rotation of the arm in space. The neural network model computes the motor command by combining the visual information about movement trajectory with the kinesthetic information concerning the orientation of the arm in space. The appropriate combination, learned by the network from spontaneous movement, can be approximated by a bilinear operation that can be interpreted as a projection of the visual information on a reference frame that rotates with the arm. This bilinear combination implies that neural circuits converging on a single neuron in the motor and premotor cortices can learn and generalize the appropriate command in a 2-D subspace but not in the whole 3-D space. However, the uniform distribution of cell preferred directions in these frontal areas can explain the computation of the correct solution by a population of cortical neurons. The model is consistent with the existing neurophysiological data and predicts how visual and somatic information can be combined in the different processing steps of the visuomotor transformation subserving visual reaching.     

A robotic manipulator for the characterization of two-dimensional dynamic stiffness using stochastic displacement perturbations

Experimental techniques for estimating the two-dimensional dynamic stiffness of the human arm over a wide range of conditions have been developed. A robotic manipulator has been developed to create loads against which subjects perform various tasks and also to impose perturbations onto the endpoint of the arm to allow estimation of its mechanical properties. The manipulator can produce static endpoint forces exceeding 220 N in any direction in its plane of motion, and this plane can be vertically translated and tilted over wide ranges to study arm dynamic stiffness in many functionally relevant planes. It can impose stochastic position and force perturbations whose bandwidth exceeds that of the arm. These random perturbations avoid undesirable volitional reactions and allow the efficient estimation of stiffness dynamics using experimental trials of short duration. The ability of this manipulator to characterize inertial-viscoelastic systems was tested using several two-dimensional physical systems whose properties were independently characterized. The endpoint dynamic stiffness properties of a human arm were estimated as an example of the use of the manipulator in studying upper limb mechanical properties. The system properties characterized by these methods will be useful in probing normal neural arm control strategies and in developing rehabilitation interventions to improve arm movements in disabled individuals.     

Adaptation motor learning of arm movements in patients with cerebellar disease.

OBJECTIVE--To design a test of motor learning using arm movements in normal subjects and patients with cerebellar disease. METHODS--Elbow angle was continuously displayed as a cursor (a dot) on a computer screen, and subjects made ballistic elbow flexion and extension movements to try to move the cursor between two targets on the screen. The relation between the arm movement and its visual feedback was changed, and the subjects reacted by adapting the amplitude of their movements in subsequent trials. RESULTS--The consecutive errors showed exponential learning curves during adaptation, which were quantified by their steepness. Ten patients with isolated cerebellar or olivopontocerebellar degeneration had less steep learning curves than normal subjects, indicating a failure of adaptation motor learning in cerebellar disease. The results show that this test may be useful for the analysis of motor learning.     

Automatic drive of limb motor plasticity

The ability to perform accurate limb movements may require learning mechanisms that continually tune the motor system. In the current study, we isolate a form of pure limb motor plasticity. Participants reached to targets that were turned off just after the onset of an initial eye movement, reappearing at a new location at the end of the reaching movement. In contrast to classical prism or virtual reality paradigms, our task eliminated sensory adaptation by always maintaining a congruency between the seen and felt limb position. We also minimized awareness and potential adaptation processes on the basis of volitional strategies by progressively increasing the size of the target perturbations. In this manner, our adaptation procedure mimicked conditions used to study saccadic adaptation. The results indicated that adaptation under these conditions led to a robust after-effect that generalized to a large range of movements within the workspace. This fully natural, nonimposed generalization of adaptation is not expressed in a spatial coordinate system, but more likely in a joint-centered coordinate space.     

Programs for action in superior parietal cortex: a triple-pulse TMS investigation

Converging evidence from neurological patients and functional brain imaging studies strongly supports the notion that the posterior parietal cortex (PPC), especially in the left hemisphere, plays a critical role in both the programming (i.e., setting the initial movement parameters of the reach) and the online control of goal-directed reaching movements. Importantly, however, there is no clear consensus on how different subregions within the PPC contribute to the programming and online control of reaching. In the current study, we investigated the role of the inferior (IPL) and superior (SPL) parietal lobules in reach programming using MRI-guided event-related transcranial magnetic stimulation (TMS). Specifically, we applied triple-pulse (tp) TMS to either the left IPL or the left SPL at different time points during reaching movements either at target onset (programming) or at movement onset (online control) while participants (n = 16) made pointing movements to targets in the periphery without visual feedback of the moving hand. Stimulating the SPL but not the IPL resulted in a significant increase in endpoint errors when tp-TMS was applied during the programming phase compared to the online control phase. In short, these data demonstrate that the SPL plays a critical role in real-time movement programming.