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Abstract Existing models of human walking use low-level reflexes or neural oscillators to generate movement. While appropriate to generate the stable, rhythmic movement patterns of steady-state walking, these models lack the ability to change their movement patterns or spontaneously generate new movements in the specific, goal-directed way characteristic of voluntary movements. Here we present a neuromuscular model of human locomotion that bridges this gap and combines the ability to execute goal directed movements with the generation of stable, rhythmic movement patterns that are required for robust locomotion. The model represents goals for voluntary movements of the swing leg on the task level of swing leg joint kinematics. Smooth movements plans towards the goal configuration are generated on the task level and transformed into descending motor commands that execute the planned movements, using internal models. The movement goals and plans are updated in real time based on sensory feedback and task constraints. On the spinal level, the descending commands during the swing phase are integrated with a generic stretch reflex for each muscle. Stance leg control solely relies on dedicated spinal reflex pathways. Spinal reflexes stimulate Hill-type muscles that actuate a biomechanical model with eight internal joints and six free-body degrees of freedom. The model is able to generate voluntary, goal-directed reaching movements with the swing leg and combine multiple movements in a rhythmic sequence. During walking, the swing leg is moved in a goal-directed manner to a target that is updated in real-time based on sensory feedback to maintain upright balance, while the stance leg is stabilized by low-level reflexes and a behavioral organization switching between swing and stance control for each leg. With this combination of reflex-based stance leg and voluntary, goal-directed control of the swing leg, the model controller generates rhythmic, stable walking patterns in which the swing leg movement can be flexibly updated in real-time to step over or around obstacles.
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A computational study of how an α- to γ-motoneurone collateral can mitigate velocity-dependent stretch reflexes during voluntary movement
The primary motor cortex does not uniquely or directly produce alpha motoneurone (α-MN) drive to muscles during voluntary movement. Rather, α-MN drive emerges from the synthesis and competition among excitatory and inhibitory inputs from multiple descending tracts, spinal interneurons, sensory inputs, and proprioceptive afferents. One such fundamental input is velocity-dependent stretch reflexes in lengthening muscles, which should be inhibited to enable voluntary movement. It remains an open question, however, the extent to which unmodulated stretch reflexes disrupt voluntary movement, and whether and how they are inhibited in limbs with numerous multiarticular muscles. We used a computational model of a Rhesus Macaque arm to simulate movements with feedforward α-MN commands only, and with added velocity-dependent stretch reflex feedback. We found that velocity-dependent stretch reflex caused movement-specific, typically large and variable disruptions to arm movements. These disruptions were greatly reduced when modulating velocity-dependent stretch reflex feedback (i) as per the commonly proposed (but yet to be clarified) idealized alpha-gamma (α-γ) coactivation or (ii) an alternative α-MN collateral projection to homonymous γ-MNs. We conclude that such α-MN collaterals are a physiologically tenable propriospinal circuit in the mammalian fusimotor system. These collaterals could still collaborate with α-γ coactivation, and the few skeletofusimotor fibers (β-MNs) in mammals, to create a flexible fusimotor ecosystem to enable voluntary movement. By locally and automatically regulating the highly nonlinear neuro-musculo-skeletal mechanics of the limb, these collaterals could be a critical low-level enabler of learning, adaptation, and performance via higher-level brainstem, cerebellar, and cortical mechanisms.
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- Award ID(s):
- 2113096
- PAR ID:
- 10565890
- Publisher / Repository:
- PNAS
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 121
- Issue:
- 34
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2321659121
