Progressive adaptation of whole-limb kinematics after peripheral nerve injury

Abstract

The ability to recover purposeful movement soon after debilitating neuromuscular injury is essential to animal survival. Various neural and mechanical mechanisms exist to preserve whole-limb kinematics despite exhibiting long-term deficits of individual joints following peripheral nerve injury. However, it is unclear whether functionally relevant whole-limb movement is acutely conserved following injury. Therefore, the objective of this longitudinal study of the injury response from four individual cats was to test the hypothesis that whole-limb length is conserved following localized nerve injury of ankle extensors in cats with intact nervous systems. The primary finding of our study was that whole-limb kinematics during walking was not immediately preserved following peripheral nerve injuries that paralyzed subsets of ankle extensor muscles. Instead, whole-limb kinematics recovered gradually over multiple weeks, despite having the mechanical capacity of injury-spared muscles across all joints to achieve immediate functional recovery. The time taken to achieve complete recovery of whole-limb kinematics is consistent with an underlying process that relies on neuromuscular adaptation. Importantly, the gradual recovery of ankle joint kinematics remained incomplete, discontinuing once whole-limb kinematics had fully recovered. These findings support the hypothesis that a whole-limb representation of healthy limb function guides a locomotor compensation strategy after neuromuscular injury that arrests progressive changes in the joint kinematics once whole-limb kinematics is regained.

Adaptation of muscle activation after patellar loading demonstrates neural control of joint variables

“…Further, those studies all examined short term effects of patellar taping, because of the difficulties in performing long term EMG recordings in humans. However, changes in EMGs in response to patellar loading, might only develop over multiple days, similar to the progressive adaptation observed in response to changes in musculoskeletal properties 13–15 . We therefore exploited the relative simplicity of the patellar mechanics in the rat and the ability to perform long term recordings of EMGs to examine whether patellar loading alters the balance of activation between VM and VL during locomotion and whether this alteration is consistent with the regulation of internal joint stresses and strains.…”

“…It is important to note, however, that the measurements taken a few hours after spring attachment could have been affected by analgesics administered following the procedures for attaching the spring that were absent at later time points. A gradual adaptation process in response to persistent alterations in mediolateral patellar forces is similar to the gradual adaptation process following injury or changes in musculoskeletal properties 13–15 . signaled directly to the CNS by sensory afferents within the knee joint 22 or indirectly by proprioceptive afferents in quadriceps muscles 23 .…”

Spinal motor circuit synaptic plasticity after peripheral nerve injury depends on microglia activation and a CCR2 mechanism

“…The physiological significance of this Ia afferent circuit plasticity in the spinal cord ventral horn is not fully clear. Loss of Ia inputs manifests in joint discoordination and diminished performance after muscles are reinnervated, in particular for motor tasks requiring fast and accurate proprioceptive feedback (Cope et al, 1994;Abelew et al, 2000;Haftel et al, 2005;Maas et al, 2007;Bullinger et al, 2011;Sabatier et al, 2011;Lyle et al, 2017;Chang et al, 2018). On the other hand, deletion of Ia/II inputs might reduce connectivity incongruences between proprioceptors and MNs inside the spinal cord after both sensory and motor axons regenerate in the periphery.…”

“…Absence of Ia input implies that ventral horn motor circuitries operate after regeneration without feedback about muscles lengths and dynamics, and force signals from Ib Golgi afferents become unopposed, both affecting many spinal control mechanisms. Thus, motor tasks involving high forces and/or rapid and large muscle lengthening (steep slopes) show deficits (Abelew et al, 2000;Maas et al, 2007;Sabatier et al, 2011;Lyle et al, 2017;Chang et al, 2018). The mechanisms implicated in this die-back of ventral horn Ia axons are unknown.…”

Synaptic Plasticity on Motoneurons After Axotomy: A Necessary Change in Paradigm

“…Its absence, however, implies that ventral horn motor circuitries operate without Ia feedback about muscle lengths and dynamics after regeneration from nerve transections, thus affecting many critical spinal control mechanisms. Accordingly, motor tasks involving high forces and/or rapid and large muscle lengthening (steep slopes) show deficits (Abelew et al, 2000;Maas et al, 2007;Sabatier et al, 2011b;Lyle et al, 2017;Chang et al, 2018). Moreover, the lack of effective Ia inputs in the ventral horn might also affect circuitries like reciprocal inhibition and explain the presence of reciprocal excitation between antagonistic muscles and higher co-contraction and joint stiffness during motor function following regeneration from nerve transections (Sabatier et al, 2011a;Horstman et al, 2019; see Figure 10 in Horstman et al, 2019 for putative circuit mechanisms).…”