Self-reinnervated muscles lose autogenic length feedback, but intermuscular feedback can recover functional connectivity

Abstract

In this study, we sought to identify sensory circuitry responsible for motor deficits or compensatory adaptations after peripheral nerve cut and repair. Self-reinnervation of the ankle extensor muscles abolishes the stretch reflex and increases ankle yielding during downslope walking, but it remains unknown whether this finding generalizes to other muscle groups and whether muscles become completely deafferented. In decerebrate cats at least 19 wk after nerve cut and repair, we examined the influence of quadriceps (Q) muscles' self-reinnervation on autogenic length feedback, as well as intermuscular length and force feedback, among the primary extensor muscles in the cat hindlimb. Effects of gastrocnemius and soleus self-reinnervation on intermuscular circuitry were also evaluated. We found that autogenic length feedback was lost after Q self-reinnervation, indicating that loss of the stretch reflex appears to be a generalizable consequence of muscle self-reinnervation. However, intermuscular force and length feedback, evoked from self-reinnervated muscles, was preserved in most of the interactions evaluated with similar relative inhibitory or excitatory magnitudes. These data indicate that intermuscular spinal reflex circuitry has the ability to regain functional connectivity, but the restoration is not absolute. Explanations for the recovery of intermuscular feedback are discussed, based on identified mechanisms responsible for lost autogenic length feedback. Functional implications, due to permanent loss of autogenic length feedback and potential for compensatory adaptations from preserved intermuscular feedback, are discussed.

Optogenetically enhanced axon regeneration: motor versus sensory neuron‐specific stimulation

“…In this same context, medium and large DRG neurons are primarily responsible for proprioceptive feedback and mechanosensation, while small DRG neurons are largely nociceptive. We (Brandt et al ., ; Cannoy et al ., ) and others (Cope et al ., ; Lyle et al ., ) have argued previously that restoration of the impact of the larger afferent neurons is an important factor in improving functional recovery after peripheral nerve injury. The promotion of regeneration of presumed proprioceptive axons by selective afferent stimulation is thus encouraging.…”

VGLUT1 synapses and P‐boutons on regenerating motoneurons after nerve crush

“…For example, full nerve transection and repair of small distal nerves projecting to single hind limb muscles (medial gastrocnemius [MG] nerve or quadriceps nerves) result in rapid and specific muscle reinnervation and full recovery of force within weeks, but stretch reflexes are permanently lost. This occurs even though stretchsensitive sensory proprioceptors (i.e., Ia afferents) efficiently reinnervate muscle spindle receptors and are capable of encoding and transmitting information about muscle length (Bullinger, Nardelli, Pinter, Alvarez, & Cope, 2011;Cope, Bonasera, & Nichols, 1994;Haftel et al, 2005;Lyle, Prilutsky, Gregor, Abelew, & Nichols, 2016). Deficits in feedback information about muscle length manifest in abnormal interjoint coordination during walking, higher than normal co-contraction of antagonists around single joints and errors in slope walking (Abelew, Miller, Cope, & Nichols, 2000;Maas, Prilutsky, Nichols, & Gregor, 2007;Sabatier, To, Nicolini, & English, 2011).…”

Musculotendon adaptations and preservation of spinal reflex pathways following agonist-to-antagonist tendon transfer

“…The details of the hardware and software used have been described previously (Wilmink and Nichols ; Ross and Nichols ; Lyle et al. ). In brief, the protocol involved 2 mm muscle stretches with a 50 msec ramp, 100 msec hold and 50 msec release.…”

“…The baseline force vectors used to remove the background force offset were determined using linear interpolation from stretch onset to a point 900 msec after stretch onset (Ross and Nichols ; Lyle et al. ). Stretch repetitions that had a sudden background force change precluding an accurate baseline force vector determination were eliminated from analysis, as were spontaneous force responses unrelated to muscle stretch or tibial nerve stimulation during a trial.…”