The Influence of Visual Perturbations on the Neural Control of Limb Stiffness

Department of Psychology, The University of Western Ontario, 1151 Richmond St., London, Ontario, Canada N6A 5C2.
Journal of Neurophysiology (Impact Factor: 2.89). 08/2008; 101(1):246-57. DOI: 10.1152/jn.90371.2008
Source: PubMed


To adapt to novel unstable environments, the motor system modulates limb stiffness to produce selective increases in arm stability. The motor system receives information about the environment via somatosensory and proprioceptive signals related to the perturbing forces and visual signals indicating deviations from an expected hand trajectory. Here we investigated whether subjects modulate limb stiffness during adaptation to a purely visual perturbation. In a first experiment, measurements of limb stiffness were taken during adaptation to an elastic force field (EF). Observed changes in stiffness were consistent with previous reports: subjects increased limb stiffness and did so only in the direction of the environmental instability. In a second experiment, stiffness changes were measured during adaptation to a visual perturbing environment that magnified hand-path deviations in the lateral direction. In contrast to the first experiment, subjects trained in this visual task showed no accompanying change in stiffness, despite reliable improvements in movement accuracy. These findings suggest that this sort of visual information alone may not be sufficient to engage neural systems for stiffness control, which may depend on sensory signals more directly related to perturbing forces, such as those arising from proprioception and somatosensation.

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    • "When the right arm was perturbed, in the former condition the response was limited to the right arm, whereas in the later condition both arms responded. In another example, Burdet et al. (2001) and others (Franklin et al., 2007; Wong et al., 2009) imposed a diverging force field on reaching movements and found that with practice, perturbation response of the arm during the reach increased along an axis that was parallel to the diverging field. Finally, when people reached in a curl field in which the forces pushed the hand in only one direction, response of the arm during the reach increased for perturbations that were parallel to the field (Wang et al., 2001; Kimura et al., 2006; Kimura and Gomi, 2009). "
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    ABSTRACT: In a voluntary movement, the nervous system specifies not only the motor commands but also the gains associated with reaction to sensory feedback. For example, suppose that, during reaching, a perturbation tends to push the hand to the left. With practice, the brain not only learns to produce commands that predictively compensate for the perturbation but also increases the long-latency reflex gain associated with leftward displacements of the arm. That is, the brain learns a feedback controller. Here, we wondered whether, during the preparatory period before the reach, the brain engaged this feedback controller in anticipation of the upcoming movement. If so, its signature might be present in how the motor system responds to perturbations in the preparatory period. Humans trained on a reach task in which they adapted to a force field. During the preparatory period before the reach, we measured how the arm responded to a pulse to the hand that was either in the direction of the upcoming field, or in the opposite direction. Reach adaptation produced an increase in the long-latency (45-100 ms delay) feedback gains with respect to baseline, but only for perturbations that were in the same direction as the force field that subjects expected to encounter during the reach. Therefore, as the brain prepares for a reach, it loads a feedback controller specific to the upcoming reach. With adaptation, this feedback controller undergoes a change, increasing the gains for the expected sensory feedback.
    The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 07/2012; 32(28):9537-45. DOI:10.1523/JNEUROSCI.4275-11.2012 · 6.34 Impact Factor
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    • "In an unstable or unpredictable environment, the central nervous system (CNS) learns to co-contract suitable muscle pairs involved in the movement (Burdet et al. 2001; Franklin et al. 2007a, 2003b) stabilizing the limb end point and minimizing the production and effect of motor noise (Selen et al. 2005, 2009). However, all previous studies investigating impedance control in reaching movements examined only a single movement direction (Burdet et al. 2001, 2006; Franklin et al. 2003a, 2008; 2007a, 2003b, 2007b; Osu et al. 2003, 2002; Takahashi et al. 2001; Wong et al. 2009a,b). Can humans learn impedance control models to compensate for different directions of instability across the workspace? "
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    ABSTRACT: Humans are able to learn tool-handling tasks, such as carving, demonstrating their competency to make movements in unstable environments with varied directions. When faced with a single direction of instability, humans learn to selectively co-contract their arm muscles tuning the mechanical stiffness of the limb end point to stabilize movements. This study examines, for the first time, subjects simultaneously adapting to two distinct directions of instability, a situation that may typically occur when using tools. Subjects learned to perform reaching movements in two directions, each of which had lateral instability requiring control of impedance. The subjects were able to adapt to these unstable interactions and switch between movements in the two directions; they did so by learning to selectively control the end-point stiffness counteracting the environmental instability without superfluous stiffness in other directions. This finding demonstrates that the central nervous system can simultaneously tune the mechanical impedance of the limbs to multiple movements by learning movement-specific solutions. Furthermore, it suggests that the impedance controller learns as a function of the state of the arm rather than a general strategy.
    Journal of Neurophysiology 08/2011; 106(5):2737-48. DOI:10.1152/jn.00079.2011 · 2.89 Impact Factor
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    • "Increased activation of the muscles around a joint may increase neuromuscular noise through increasing force variability (Meulenbroek et al. 2005; Faisal et al. 2008), but stiffening at a joint also increases stabilization (Gribble et al. 2003; Faisal et al. 2008; Selen et al. 2009). Thus, the choice of limiting motion at the ankle and hip may be an attempt by older women to decrease sensorymotor noise and enhance behavioral precision for the somatosensory disturbances (Wong et al. 2009). "
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    ABSTRACT: The effect of continuous visual flow on the ability to regain and maintain postural orientation was examined. Fourteen young (20-39 years old) and 14 older women (60-79 years old) stood quietly during 3° (30°/s) dorsiflexion tilt of the support surface combined with 30° and 45°/s upward or downward pitch rotations of the visual field. The support surface was held tilted for 30 s and then returned to neutral over a 30-s period while the visual field continued to rotate. Segmental displacement and bilateral tibialis anterior and gastrocnemius muscle EMG responses were recorded. Continuous wavelet transforms were calculated for each muscle EMG response. An instantaneous mean frequency curve (IMNF) of muscle activity, center of mass (COM), center of pressure (COP), and angular excursion at the hip and ankle were used in a functional principal component analysis (fPCA). Functional component weights were calculated and compared with mixed model repeated measures ANOVAs. The fPCA revealed greatest mathematical differences in COM and COP responses between groups or conditions during the period that the platform transitioned from the sustained tilt to a return to neutral position. Muscle EMG responses differed most in the period following support surface tilt indicating that muscle activity increased to support stabilization against the visual flow. Older women exhibited significantly larger COM and COP responses in the direction of visual field motion and less muscle modulation when the platform returned to neutral than younger women. Results on a Rod and Frame test indicated that older women were significantly more visually dependent than the younger women. We concluded that a stiffer body combined with heightened visual sensitivity in older women critically interferes with their ability to counteract posturally destabilizing environments.
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