While the study of unconstrained movements has revealed important features of neural control, generalizing those insights to more sophisticated object manipulation is challenging. Humans excel at physical interaction with objects, even when those objects introduce complex dynamics and kinematic constraints. This study examined humans turning a horizontal planar crank (radius 10.29 cm) at their preferred and three instructed speeds (with visual feedback), both in clockwise and counterclockwise directions. To explore the role of neuromechanical dynamics, the instructed speeds covered a wide range: fast (near the limits of performance), medium (near preferred speed), and very slow (rendering dynamic effects negligible). Because kinematically constrained movements involve significant physical interaction, disentangling neural control from the influences of biomechanics presents a challenge. To address it, we modeled the interactive dynamics to “subtract off” peripheral biomechanics from observed force and kinematic data, thereby estimating aspects of underlying neural action that may be expressed in terms of motion. We demonstrate the value of this method: remarkably, an approximately elliptical path emerged, and speed minima coincided with curvature maxima, similar to what is seen in unconstrained movements, even though the hand moved at nearly constant speed along a constant-curvature path. These findings suggest that the neural controller takes advantage of peripheral biomechanics to simplify physical interaction. As a result, patterns seen in unconstrained movements persist even when physical interaction prevents their expression in hand kinematics. The reemergence of a speed-curvature relation indicates that it is due, at least in part, to neural processes that emphasize smoothness and predictability. NEW & NOTEWORTHY Physically interacting with kinematic constraints is commonplace in everyday actions. We report a study of humans turning a crank, a circular constraint that imposes constant hand path curvature and hence should suppress variations of hand speed due to the power-law speed-curvature relation widely reported for unconstrained motions. Remarkably, we found that, when peripheral biomechanical factors are removed, a speed-curvature relation reemerges, indicating that it is, at least in part, of neural origin.
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Neuromechanical wave resonance in jellyfish swimming
For organisms to have robust locomotion, their neuromuscular organization must adapt to constantly changing environments. In jellyfish, swimming robustness emerges when marginal pacemakers fire action potentials throughout the bell’s motor nerve net, which signals the musculature to contract. The speed of the muscle activation wave is dictated by the passage times of the action potentials. However, passive elastic material properties also influence the emergent kinematics, with time scales independent of neuromuscular organization. In this multimodal study, we examine the interplay between these two time scales during turning. A three-dimensional computational fluid–structure interaction model of a jellyfish was developed to determine the resulting emergent kinematics, using bidirectional muscular activation waves to actuate the bell rim. Activation wave speeds near the material wave speed yielded successful turns, with a 76-fold difference in turning rate between the best and worst performers. Hyperextension of the margin occurred only at activation wave speeds near the material wave speed, suggesting resonance. This hyperextension resulted in a 34-fold asymmetry in the circulation of the vortex ring between the inside and outside of the turn. Experimental recording of the activation speed confirmed that jellyfish actuate within this range, and flow visualization using particle image velocimetry validated the corresponding fluid dynamics of the numerical model. This suggests that neuromechanical wave resonance plays an important role in the robustness of an organism’s locomotory system and presents an undiscovered constraint on the evolution of flexible organisms. Understanding these dynamics is essential for developing actuators in soft body robotics and bioengineered pumps.
more » « less- NSF-PAR ID:
- 10216679
- Publisher / Repository:
- Proceedings of the National Academy of Sciences
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 11
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- Article No. e2020025118
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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