Human motor behavior is constantly adapted through the process of error-based learning. When the motor system encounters an error, its estimate about the body and environment will change, and the next movement will be immediately modified to counteract the underlying perturbation. Here, we show that a second mechanism, use-dependent learning, simultaneously changes movements to become more similar to the last movement. In three experiments, participants made reaching movements toward a horizontally elongated target, such that errors in the initial movement direction did not have to be corrected. Along this task-redundant dimension, we were able to induce use-dependent learning by passively guiding movements in a direction angled by 8°from the previous direction. In a second study, we show that error-based and use-dependent learning can change motor behavior simultaneously in opposing directions by physically constraining the direction of active movements. After removal of the constraint, participants briefly exhibit an error-based aftereffect against the direction of the constraint, followed by a longer-lasting use-dependent aftereffect in the direction of the constraint. In the third experiment, we show that these two learning mechanisms together determine the solution the motor system adopts when learning a motor task.
Investigating cyclic vertical arm movements with an instrumented hand-held load in an airplane undergoing parabolic flight profiles allowed us to determine how humans modulate their grip force when the gravitational and the inertial components of the load force are varied independently. Eight subjects participated in this study; four had already experienced parabolic flights and four had not. The subjects were asked to move the load up and down continuously at three different gravitational conditions (1 g, 1.8 g, and 0 g). At 1 g, the grip force precisely anticipated the fluctuations in the load force, which was maximum at the bottom of the object trajectory and minimum at the top. When gravity changed, the temporal coupling between grip force and load force persisted for all subjects from the first parabola. At 0 g, the grip force was accurately adjusted to the two load force peaks occurring at the two opposite extremes of the trajectory due to the absence of weight. While the experienced subjects exerted a grip force appropriate to a new combination of weight and inertia since their first trial, the inexperienced subjects dramatically increased their grip when faced with either high or low force levels for the first time. Then they progressively released their grip until a continuous grip-load force relationship with regard to 1 g was established after the fifth parabola. We suggest that a central representation of the new gravitational field was rapidly acquired through the incoming vestibular and somatic sensory information.
Redundancy is a fundamental feature of biological motor systems. For example, when touching an object, many different combinations of movements of the shoulder, elbow, wrist, and finger joints result in the same movement at the fingertip. Exploiting this redundancy, the motor system distributes work across effectors to minimize signal-dependent noise and effort. When an error occurs, however, the motor system must assign the error to specific effectors, even though it may be ambiguous which effector caused them. Here, we studied the principles of responsibility assignment by using a bimanual task, in which the left and right hands jointly moved a visual cursor. We found that participants assigned errors, which were induced by visual rotation of the cursor, in a unified manner for correction and adaptation; the hand that corrected more for the error within the current movement also showed a bigger adaptive change in the next movement. Right-handed participants corrected errors more with their left hands, even though they corrected faster with their right hands in nonredundant tasks. Further experiments show that the motor system assigns responsibility preferentially to the hand that was previously exposed to larger errors. Our results show that responsibility assignment is a flexible process that attributes errors to the most likely cause.
In this experiment we examined the coupling between grip force and load force observed during cyclic vertical arm movements with a hand-held object, performed in different gravitational environments. Six subjects highly experienced in parabolic flight participated in this study. They had to continuously move a cylindrical object up and down in the different gravity fields (1g, 1.8 g and 0 g) induced by parabolic flights. The imposed movement frequency was 1 Hz, the object mass was either 200 or 400 g, the amplitude of movement was either 20 or 40 cm and an additional mass of 200 g could be wound around the forearm. Each subject performed the task during 15 consecutive parabolas. The coordination between the grip force normal to the surface and the tangential load force was examined in nine loading conditions. We observed that the same normal grip force was used for equivalent loads generated by changes of mass, gravity or acceleration despite the fact that these loads required different motor commands to move the arm. Moreover, our results suggest that the gravitational and inertial components of the load are treated adequately and independently by the internal models used to predictively control the required grip force. These results indicate that the forward internal models used to control precision grip take into account the dynamic characteristics of the upper limb, the object and the environment to predict the object's acceleration and, in turn, the load force acting at the fingertips.
White O, Bleyenheuft Y, Ronsse R, Smith AM, Thonnard J-L, Lefèvre P. Altered gravity highlights central pattern generator mechanisms. J Neurophysiol 100: 2819 -2824, 2008. First published July 23, 2008 doi:10.1152/jn.90436.2008. In many nonprimate species, rhythmic patterns of activity such as locomotion or respiration are generated by neural networks at the spinal level. These neural networks are called central pattern generators (CPGs). Under normal gravitational conditions, the energy efficiency and the robustness of human rhythmic movements are due to the ability of CPGs to drive the system at a pace close to its resonant frequency. This property can be compared with oscillators running at resonant frequency, for which the energy is optimally exchanged with the environment. However, the ability of the CPG to adapt the frequency of rhythmic movements to new gravitational conditions has never been studied. We show here that the frequency of a rhythmic movement of the upper limb is systematically influenced by the different gravitational conditions created in parabolic flight. The period of the arm movement is shortened with increasing gravity levels. In weightlessness, however, the period is more dependent on instructions given to the participants, suggesting a decreased influence of resonant frequency. Our results are in agreement with a computational model of a CPG coupled to a simple pendulum under the control of gravity. We demonstrate that the innate modulation of rhythmic movements by CPGs is highly flexible across gravitational contexts. This further supports the involvement of CPG mechanisms in the achievement of efficient rhythmic arm movements. Our contribution is of major interest for the study of human rhythmic activities, both in a normal Earth environment and during microgravity conditions in space.
Mental imagery is a cognitive tool that helps humans take decisions by simulating past and future events. The hypothesis has been advanced that there is a functional equivalence between actual and mental movements. Yet, we do not know whether there are any limitations to its validity even in terms of some fundamental features of actual movements, such as the relationship between space and time. Although it is impossible to directly measure the spatiotemporal features of mental actions, an indirect investigation can be conducted by taking advantage of the constraints existing in planar drawing movements and described by the two-thirds power law (2/3PL). This kinematic law describes one of the most impressive regularities observed in biological movements: movement speed decreases when curvature increases. Here, we compared the duration of identical actual and mental arm movements by changing the constraints imposed by the 2/3PL. In the first two experiments, the length of the trajectory remained constant, while its curvature (Experiment 1) or its number of inflexions (Experiment 2) was manipulated. The results showed that curvature, but not the number of inflexions, proportionally and similarly affected actual and mental movement duration, as expected from the 2/3PL. Two other control experiments confirmed that the results of Experiment 1 were not attributable to eye movements (Experiment 3) or to the perceived length of the displayed trajectory (Experiment 4). Altogether, our findings suggest that mental movement simulation is tuned to the kinematic laws characterizing actions and that kinematics of actual and mental movements is completely specified by the representation of their geometry.
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