Swing Velocity Profiles of Small Limbs Can Arise from Transient Passive Torques of the Antagonist Muscle Alone

In large limbs, changing motor neuron activity typically controls within-movement velocity. For example, sequential agonist-antagonist-agonist motor neuron firing typically underlies the slowing often present at the end of human reaches. In physiological movements of large limbs, antagonistic muscle passive torque is generally negligible. In small limbs, alternatively, passive torques can determine limb rest position, generate restoring movements to it, and decrease agonist-generated movement amplitude and velocity maxima. These observations suggest that in small limbs passive forces might also control velocity changes within movements. We investigated this issue in stick insect middle leg femur-tibia (FT) joint. During swing, the FT joint extensor muscle actively shortens and the flexor muscle passively lengthens. As in human reaching, after its initial acceleration, FT joint velocity continuously decreases. We measured flexor passive forces during imposed stretches spanning the ranges of FT joint angles, angular velocities, and movement amplitudes present in leg swings. The viscoelastic “transient” passive force that occurs during and soon after stretch depended on all three variables, and could be tens of times larger than the “steady-state” passive force commonly measured long after stretch end. We combined these data, the flexor and extensor moment arms, and an existing extensor model to simulate FT joint swing. To measure only passive (flexor) muscle-dependent effects, we used constant extensor activations in these simulations. In simulations using data from ten flexor muscles, flexor passive torque could always produce swings with, after swing initiation, continuously decreasing velocities. Antagonist muscle passive torques alone can thus control within-movement velocity.在大型肢体中，运动神经元活动的改变通常调控运动过程中的速度变化。例如，主动肌（agonist）-拮抗肌（antagonist）-主动肌依次放电的运动神经元活动模式，通常是人类伸手动作末期常见的速度减缓现象的基础。在大型肢体的生理性运动中，拮抗肌的被动力矩通常可忽略不计。与之相反，在小型肢体中，被动力矩可决定肢体的静息位置，产生朝向该位置的复位运动，并降低主动肌产生的运动幅度与最大速度。上述观察结果表明，在小型肢体中，被动力或许同样能够调控运动过程中的速度变化。我们以竹节虫（stick insect）的中足股胫（femur-tibia, FT）关节为对象开展了相关研究。在摆动阶段，FT关节的伸肌（extensor muscle）会主动收缩变短，而屈肌（flexor muscle）则被动拉长。与人类伸手动作类似，FT关节的速度在初始加速后会持续下降。我们在施加牵伸的过程中测量了屈肌的被动力，牵伸覆盖了腿部摆动时FT关节的角度、角速度以及运动幅度的范围。牵伸过程中及牵伸结束后不久产生的粘弹性“瞬态”被动力，受上述三个变量共同影响，其大小可比牵伸结束很久后通常测得的“稳态”被动力大数十倍。我们将这些数据、屈肌与伸肌的肌力矩臂（moment arms），以及已有的伸肌模型相结合，对FT关节的摆动过程进行了模拟。为了仅衡量依赖于被动（屈肌）的效应，我们在这些模拟中采用了恒定的伸肌激活水平。在使用10块屈肌的数据进行的模拟中，屈肌的被动力矩始终能够产生摆动过程，且在摆动启动后速度持续下降。由此可见，仅依靠拮抗肌的被动力矩，即可调控运动过程中的速度变化。