Motor learning is dependent upon plasticity in motor areas of the brain, but does it occur in isolation, or does it also result in changes to sensory systems? We examined changes to somatosensory function that occur in conjunction with motor learning. We found that even after periods of training as brief as 10 min, sensed limb position was altered and the perceptual change persisted for 24 h. The perceptual change was reflected in subsequent movements; limb movements following learning deviated from the prelearning trajectory by an amount that was not different in magnitude and in the same direction as the perceptual shift. Crucially, the perceptual change was dependent upon motor learning. When the limb was displaced passively such that subjects experienced similar kinematics but without learning, no sensory change was observed. The findings indicate that motor learning affects not only motor areas of the brain but changes sensory function as well.
Motor learning changes the activity of cortical motor and subcortical areas of the brain, but does learning affect sensory systems as well? We examined in humans the effects of motor learning using fMRI measures of functional connectivity under resting conditions, and found persistent changes in networks involving both motor and somatosensory areas of the brain. We developed a technique that allows us to distinguish changes in functional connectivity that can be attributed to motor learning from those that are related to perceptual changes that occur in conjunction with learning. Using this technique, we identified a new network in motor learning involving second somatosensory cortex, ventral premotor cortex and supplementary motor cortex whose activation is specifically related to perceptual changes that occur in conjunction with motor learning. We also found changes in a network comprising cerebellar cortex, primary motor and dorsal premotor cortex that were linked to the motor aspects of learning. In each network, we observed highly reliable linear relationships between neuroplastic changes and behavioral measures of either motor learning or perceptual function. Motor learning thus results in functionally specific changes to distinct resting-state networks in the brain.
The early stages of motor skill acquisition are often marked by uncertainty about the sensory and motor goals of the task, as is the case in learning to speak or learning the feel of a good tennis serve. Here we present an experimental model of this early learning process, in which targets are acquired by exploration and reinforcement rather than sensory error. We use this model to investigate the relative contribution of motor and sensory factors to human motor learning. Participants make active reaching movements or matched passive movements to an unseen target using a robot arm. We find that learning through passive movements paired with reinforcement is comparable with learning associated with active movement, both in terms of magnitude and durability, with improvements due to training still observable at a 1 week retest. Motor learning is also accompanied by changes in somatosensory perceptual acuity. No stable changes in motor performance are observed for participants that train, actively or passively, in the absence of reinforcement, or for participants who are given explicit information about target position in the absence of somatosensory experience. These findings indicate that the somatosensory system dominates learning in the early stages of motor skill acquisition.
As we begin to acquire a new motor skill, we face the dual challenge of determining and refining the somatosensory goals of our movements and establishing the best motor commands to achieve our ends. The two typically proceed in parallel, and accordingly it is unclear how much of skill acquisition is a reflection of changes in sensory systems and how much reflects changes in the brain's motor areas. Here we have intentionally separated perceptual and motor learning in time so that we can assess functional changes to human sensory and motor networks as a result of perceptual learning. Our subjects underwent fMRI scans of the resting brain before and after a somatosensory discrimination task. We identified changes in functional connectivity that were due to the effects of perceptual learning on movement. For this purpose, we used a neural model of the transmission of sensory signals from perceptual decision making through to motor action. We used this model in combination with a partial correlation technique to parcel out those changes in connectivity observed in motor systems that could be attributed to activity in sensory brain regions. We found that, after removing effects that are linearly correlated with somatosensory activity, perceptual learning results in changes to frontal motor areas that are related to the effects of this training on motor behavior and learning. This suggests that perceptual learning produces changes to frontal motor areas of the brain and may thus contribute directly to motor learning.
Darainy, Mohammad, Nicole Malfait, Paul L. Gribble, Farzad Towhidkhah, and David J. Ostry. Learning to control arm stiffness under static conditions. J Neurophysiol 92: 3344 -3350, 2004. First published July 28, 2004 doi:10.1152/jn.00596.2004. We used a robotic device to test the idea that impedance control involves a process of learning or adaptation that is acquired over time and permits the voluntary control of the pattern of stiffness at the hand. The tests were conducted in statics. Subjects were trained over the course of 3 successive days to resist the effects of one of three different kinds of mechanical loads: single axis loads acting in the lateral direction, single axis loads acting in the forward/backward direction, and isotropic loads that perturbed the limb in eight directions about a circle. We found that subjects in contact with single axis loads voluntarily modified their hand stiffness orientation such that changes to the direction of maximum stiffness mirrored the direction of applied load. In the case of isotropic loads, a uniform increase in endpoint stiffness was observed. Using a physiologically realistic model of two-joint arm movement, the experimentally determined pattern of impedance change could be replicated by assuming that coactivation of elbow and double joint muscles was independent of coactivation of muscles at the shoulder. Moreover, using this pattern of coactivation control we were able to replicate an asymmetric pattern of rotation of the stiffness ellipse that was observed empirically. These findings are consistent with the idea that arm stiffness is controlled through the use of at least two independent co-contraction commands.
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