Article

Spatially selective enhancement of proprioceptive acuity following motor learning.

Department of Psychology, The University of Western Ontario, 1151 Richmond St., London, ON Canada.
Journal of Neurophysiology (Impact Factor: 3.04). 03/2011; 105(5):2512-21. DOI: 10.1152/jn.00949.2010
Source: PubMed

ABSTRACT It is well recognized that the brain uses sensory information to accurately produce motor commands. Indeed, most research into the relationship between sensory and motor systems has focused on how sensory information modulates motor function. In contrast, recent studies have begun to investigate the reverse: how sensory and perceptual systems are tuned based on motor function, and specifically motor learning. In the present study we investigated changes to human proprioceptive acuity following recent motor learning. Sensitivity to small displacements of the hand was measured before and after 10 min of motor learning, during which subjects grasped the handle of a robotic arm and guided a cursor to a series of visual targets randomly located within a small workspace region. We used a novel method of assessing proprioceptive acuity that avoids active movement, interhemispheric transfer, and intermodality coordinate transformations. We found that proprioceptive acuity improved following motor learning, but only in the region of the arm's workspace explored during learning. No proprioceptive improvement was observed when motor learning was performed in a different location or when subjects passively experienced limb trajectories matched to those of subjects who actively performed motor learning. Our findings support the idea that sensory changes occur in parallel with changes to motor commands during motor learning.

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    • "The test procedure has been described elsewhere [11] [12] [13]. Briefly, we employed a two-alternative forced-choice paradigm to estimate the psychophysical relationship between actual and perceived position of the limb(s). "
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    ABSTRACT: Information about the position of an object that is held in both hands, such as a golf club or a tennis racquet, is transmitted to the human central nervous system from peripheral sensors in both left and right arms. How does the brain combine these two sources of information? Using a robot to move participant's passive limbs, we performed psychophysical estimates of proprioceptive function for each limb independently, and again when subjects grasped the robot handle with both arms. We compared empirical estimates of bimanual proprioception to several models from the sensory integration literature: some that propose a combination of signals from the left and right arms (such as a Bayesian maximum-likelihood estimate), and some that propose using unimanual signals alone. Our results are consistent with the hypothesis that the nervous system both has knowledge of, and uses the limb with the best proprioceptive acuity for bimanual proprioception. Surprisingly, a Bayesian model that postulates optimal combination of sensory signals could not predict empirically observed bimanual acuity. These findings suggest that while the central nervous system seems to have information about the relative sensory acuity of each limb, it uses this information in a rather rudimentary fashion, essentially ignoring information from the less reliable limb.
    Journal of Neurophysiology 12/2013; 111(6). DOI:10.1152/jn.00537.2013 · 3.04 Impact Factor
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    • "Several studies have also shown that motor learning is accompanied by adaptation in sensory systems. Learning tasks involving arm movements have been shown to change attributes of sensory function such as sensed limb position (Cressman and Henriques 2009; Haith et al. 2008; Ostry et al. 2010) and perceptual acuity (Wong et al. 2011). At the neural level, a network has been identified that is associated with the perceptual changes that occur in conjunction with motor learning. "
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    ABSTRACT: Observing the actions of others has been shown to affect motor learning, but does it have effects on sensory systems as well? It has been recently shown that motor learning that involves actual physical practice is also associated with plasticity in the somatosensory system. Here, we assessed the idea that observational learning likewise changes somatosensory function. We evaluated changes in somato-sensory function after human subjects watched videos depicting motor learning. Subjects first observed video recordings of reaching move-ments either in a clockwise or counterclockwise force field. They were then trained in an actual force-field task that involved a counterclock-wise load. Measures of somatosensory function were obtained before and after visual observation and also following force-field learning. Consistent with previous reports, video observation promoted motor learning. We also found that somatosensory function was altered following observational learning, both in direction and in magnitude, in a manner similar to that which occurs when motor learning is achieved through actual physical practice. Observation of the same sequence of movements in a randomized order did not result in somatosensory perceptual change. Observational learning and real physical practice appear to tap into the same capacity for sensory change in that subjects that showed a greater change following ob-servational learning showed a reliably smaller change following phys-ical motor learning. We conclude that effects of observing motor learning extend beyond the boundaries of traditional motor circuits, to include somatosensory representations. observational learning; somatosensory plasticity; motor learning; force-field learning OBSERVING OTHERS WHILE THEY learn a motor task has been shown to engage the motor system and to result in reliable changes to motor learning. Here, we assess the possibility that the effects of observing motor learning are not solely confined to the motor system but spread as well to somatosensory representations. We show that there are changes to sensed limb position following observational learning that are similar to those that occur follow-ing actual motor learning. There have been a number of demonstrations that motor learning can occur even in the absence of overt physical practice, as is the case of when one observes motor learning. A series of studies (Brown et al. 2009; Mattar and Gribble 2005) have shown that subjects who observed a video depicting another person learning to reach in a novel mechanical envi-ronment performed better when later tested in the same envi-ronment than subjects who observed similar movements that did not involve learning. Similarly, the observation of another individual performing repetitive thumb movements has been shown to alter both the movements and the motor potentials evoked from the stimulation of motor cortex (Stefan et al. 2005). Several studies have shown that similar brain networks are activated during the observation and execution of move-ment, in particular, ventral premotor cortex and supplementary motor area and inferior parietal lobule and superior temporal sulcus (see Kilner 2011 for review). Several studies have also shown that motor learning is accom-panied by adaptation in sensory systems. Learning tasks involving arm movements have been shown to change attributes of sensory function such as sensed limb position (Cressman and Henriques 2009; Haith et al. 2008; Ostry et al. 2010) and perceptual acuity (Wong et al. 2011). At the neural level, a network has been identified that is associated with the perceptual changes that occur in conjunction with motor learning. This comprises second so-matosensory cortex, ventral premotor cortex, and supplementary motor area (Vahdat et al. 2011). Taken together, these observations raise the possibility that changes in sensory perception could be triggered not only by actual motor learning, but also by observing someone else engaged in a motor-learning task. We tested this hypothesis by assessing somatosensory perception before and after a task that involved observation of motor learning. The test involved two groups of subjects that watched a video depicting an actor learning to reach in a novel mechanical environment. The direction of the perturbation applied to the actor's arm was opposite for the two groups. We found that watching someone else learn not only affected the characteristics of motor learn-ing, but also was associated with changes in somatosensory perception. Moreover, depending on the direction of the force field during the observed learning, the two groups showed changes in sensory perception in opposite directions. The perceptual changes observed here are in the same direction as those previously described following actual motor learning. We conclude that observational learning has effects that spread beyond motor circuits of the brain and contributes to plasticity in sensory systems.
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    • "Several studies have also shown that motor learning is accompanied by adaptation in sensory systems. Learning tasks involving arm movements have been shown to change attributes of sensory function such as sensed limb position (Cressman and Henriques 2009; Haith et al. 2008; Ostry et al. 2010) and perceptual acuity (Wong et al. 2011). At the neural level, a network has been identified that is associated with the perceptual changes that occur in conjunction with motor learning. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Observing the actions of others has been shown to affect motor learning, but does it have effects on sensory systems as well? It has been recently shown that motor learning that involves actual physical practice is also associated with plasticity in the somatosensory system. Here we assessed the idea that observational learning likewise changes somatosensory function. We evaluated changes in somatosensory function after human subjects watched videos depicting motor learning. Subjects first observed video recordings of reaching movements, either in a clock-wise or counter-clockwise force-field. They were then trained in an actual force-field task that involved a counter-clockwise load. Measures of somatosensory function were obtained before and after visual observation and also following force-field learning. Consistent with previous reports, video observation promoted motor learning. We also found that somatosensory function was altered following observational learning, both in direction and in magnitude, in a manner similar to that which occurs when motor learning is achieved through actual physical practice. Observation of the same sequence of movements in a randomized order did not result in somatosensory perceptual change. Observational learning and real physical practice appear to tap into the same capacity for sensory change in that subjects that showed a greater change following observational learning showed a reliably smaller change following physical motor learning. We conclude that effects of observing motor learning extend beyond the boundaries of traditional motor circuits, to include somatosensory representations.
    Journal of Neurophysiology 07/2013; 110(8). DOI:10.1152/jn.01061.2012 · 3.04 Impact Factor
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