Interactions Between Limb and Environmental Mechanics Influence Stretch Reflex Sensitivity in the Human Arm

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Hu X, Murray WM, Perreault EJ. Muscle short-range stiffness can be used to estimate the endpoint stiffness of the human arm. J Neurophysiol 105: 1633-1641, 2011. First published February 2, 2011 doi:10.1152/jn.00537.2010.-The mechanical properties of the human arm are regulated to maintain stability across many tasks. The static mechanics of the arm can be characterized by estimates of endpoint stiffness, considered especially relevant for the maintenance of posture. At a fixed posture, endpoint stiffness can be regulated by changes in muscle activation, but which activation-dependent muscle properties contribute to this global measure of limb mechanics remains unclear. We evaluated the role of muscle properties in the regulation of endpoint stiffness by incorporating scalable models of muscle stiffness into a three-dimensional musculoskeletal model of the human arm. Two classes of muscle models were tested: one characterizing short-range stiffness and two estimating stiffness from the slope of the force-length curve. All models were compared with previously collected experimental data describing how endpoint stiffness varies with changes in voluntary force. Importantly, muscle properties were not fit to the experimental data but scaled only by the geometry of individual muscles in the model. We found that forcedependent variations in endpoint stiffness were accurately described by the short-range stiffness of active arm muscles. Over the wide range of evaluated arm postures and voluntary forces, the musculoskeletal model incorporating short-range stiffness accounted for 98 Ϯ 2, 91 Ϯ 4, and 82 Ϯ 12% of the variance in stiffness orientation, shape, and area, respectively, across all simulated subjects. In contrast, estimates based on muscle force-length curves were less accurate in all measures, especially stiffness area. These results suggest that muscle short-range stiffness is a major contributor to endpoint stiffness of the human arm. Furthermore, the developed model provides an important tool for assessing how the nervous system may regulate endpoint stiffness via changes in muscle activation. musculoskeletal model WE COMMONLY USE OUR HANDS to move and manipulate objects in different environments. Many of these tasks tend to destabilize arm posture (Rancourt and Hogan 2001). Nevertheless, they can be completed because the central nervous system regulates the mechanical properties of the arm to compensate for these instabilities, usually ensuring that the coupled system of the arm and its environment remains stable so that posture can be maintained (McIntyre et al. 1996). Understanding how this regulation occurs and the relative contributions of the nervous system and the intrinsic biomechanics of the arm remains an important problem in motor control.

Section: Discussionmentioning

confidence: 97%

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confidence: 99%

Muscle short-range stiffness can be used to estimate the endpoint stiffness of the human arm

Murray

Perreault

2011

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“…For example, spinal reflexes of the arm can counter mechanical perturbations in as little as 20 -40 ms. These purely spinal processes are followed by long-latency responses (50 -105 ms) that can be modulated by explicit task goals (Crago et al 1976;Marsden et al 1981;Mutha et al 2008;Pruszynski et al 2008;Rothwell et al 1980) and use internal models of limb and environmental dynamics (Gielen et al 1988;Kimura and Gomi 2009;Krutky et al 2010;Kurtzer et al 2008Kurtzer et al , 2009Soechting and Lacquaniti 1988). In this respect, the capabilities of longlatency responses mirror those shown in voluntary control.…”

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confidence: 99%

Fast corrective responses are evoked by perturbations approaching the natural variability of posture and movement tasks

Crevecoeur

Kurtzer

Scott

2012

Crevecoeur F, Kurtzer I, Scott SH. Fast corrective responses are evoked by perturbations approaching the natural variability of posture and movement tasks. J Neurophysiol 107: 2821-2832, 2012. First published February 22, 2012 doi:10.1152/jn.00849.2011.-A wealth of studies highlight the importance of rapid corrective responses during voluntary motor tasks. These studies used relatively large perturbations to evoke robust muscle activity. Thus it remains unknown whether these corrective responses (latency 20 -100 ms) are evoked at perturbation levels approaching the inherent variability of voluntary control. To fill this gap, we examined responses for large to small perturbations applied while participants either performed postural or reaching tasks. To address multijoint corrective responses, we induced various amounts of single-joint elbow motion with scaled amounts of combined elbow and shoulder torques. Indeed, such perturbations are known to elicit a response at the unstretched shoulder muscle, which reflects an internal model of arm intersegmental dynamics. Significant muscle responses were observed during both postural control and reaching, even when perturbation-related joint angle, velocity, and acceleration overlapped in distribution with deviations encountered in unperturbed trials. The response onsets were consistent across the explored range of perturbation loads, with short-latency onset for the muscles spanning the elbow joints (20 -40 ms), and long-latency for shoulder muscles (onset Ͼ 45 ms). In addition, the evoked activity was strongly modulated by perturbation magnitude. These results suggest that multijoint responses are not specifically engaged to counter motor errors that exceed a certain threshold. Instead, we suggest that these corrective processes operate continuously during voluntary motor control. feedback control; internal models; long-latency reflex; motor variability; upper limb

“…This position is supported by many demonstrations that muscular activity 50 -100 ms after a mechanical perturbation (i.e., the long-latency stretch response) shows a range of modulation that reflects voluntary motor control (for review see Pruszynski and Scott 2012;Shemmell et al 2010). Such modulation of the long-latency stretch response reflects sensitivity to task demands (Dietz et al 1994;Doemges andRack 1992a, 1992b;Hager-Ross et al 1996;Marsden et al 1981;Nashed et al 2012), movement decision-making processes (Nashed et al 2014;Selen et al 2012;Yang et al 2011), routing of sensory information across different muscles (Cole et al 1984;Dimitriou et al 2012;Marsden et al 1981;Mutha and Sainburg 2009;Ohki and Johansson 1999;Omrani et al 2013), as well as knowledge of the mechanical properties of the arm (Crevecoeur et al 2012;Crevecoeur and Scott 2013;Gielen et al 1988;Koshland et al 1991;Kurtzer et al 2008Kurtzer et al , 2009Kurtzer et al , 2013Kurtzer et al , 2014Pruszynski et al 2011a;Soechting and Lacquaniti 1988) and environment (Ahmadi-Pajouh et al 2012;Akazawa et al 1983;Bedingham and Tatton 1984;Cluff and Scott 2013;Dietz et al 1994;Kimura et al 2006;Krutky et al 2010;Perreault et al 2008;Pruszynski et al 2009;Shemmell et al 2009<...>…”

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confidence: 99%

Goal-dependent modulation of the long-latency stretch response at the shoulder, elbow, and wrist

Weiler

Gribble

Pruszynski

2015

Weiler J, Gribble PL, Pruszynski JA. Goal-dependent modulation of the long-latency stretch response at the shoulder, elbow, and wrist. J Neurophysiol 114: 3242-3254, 2015. First published October 7, 2015 doi:10.1152/jn.00702.2015.-Many studies have demonstrated that muscle activity 50 -100 ms after a mechanical perturbation (i.e., the long-latency stretch response) can be modulated in a manner that reflects voluntary motor control. These previous studies typically assessed modulation of the long-latency stretch response from individual muscles rather than how this response is concurrently modulated across multiple muscles. Here we investigated such concurrent modulation by having participants execute goal-directed reaches to visual targets after mechanical perturbations of the shoulder, elbow, or wrist while measuring activity from six muscles that articulate these joints. We found that shoulder, elbow, and wrist muscles displayed goal-dependent modulation of the long-latency stretch response, that the relative magnitude of participants' goal-dependent activity was similar across muscles, that the temporal onset of goal-dependent muscle activity was not reliably different across the three joints, and that shoulder muscles displayed goal-dependent activity appropriate for counteracting intersegmental dynamics. We also observed that the long-latency stretch response of wrist muscles displayed goal-dependent modulation after elbow perturbations and that the long-latency stretch response of elbow muscles displayed goal-dependent modulation after wrist perturbations. This pattern likely arises because motion at either joint could bring the hand to the visual target and suggests that the nervous system rapidly exploits such simple kinematic redundancy when processing sensory feedback to support goal-directed actions.