Locomotor training alters the behavior of flexor reflexes during walking in human spinal cord injury

Abstract

In humans, a chronic spinal cord injury (SCI) impairs the excitability of pathways mediating early flexor reflexes and increases the excitability of late, long-lasting flexor reflexes. We hypothesized that in individuals with SCI, locomotor training will alter the behavior of these spinally mediated reflexes. Nine individuals who had either chronic clinically motor complete or incomplete SCI received an average of 44 locomotor training sessions. Flexor reflexes, elicited via sural nerve stimulation of the right or left leg, were recorded from the ipsilateral tibialis anterior (TA) muscle before and after body weight support (BWS)-assisted treadmill training. The modulation pattern of the ipsilateral TA responses following innocuous stimulation of the right foot was also recorded in 10 healthy subjects while they stepped at 25% BWS to investigate whether body unloading during walking affects the behavior of these responses. Healthy subjects did not receive treadmill training. We observed a phase-dependent modulation of early TA flexor reflexes in healthy subjects with reduced body weight during walking. The early TA flexor reflexes were increased at heel contact, progressively decreased during the stance phase, and then increased throughout the swing phase. In individuals with SCI, locomotor training induced the reappearance of early TA flexor reflexes and changed the amplitude of late TA flexor reflexes during walking. Both early and late TA flexor reflexes were modulated in a phase-dependent pattern after training. These new findings support the adaptive capability of the injured nervous system to return to a prelesion excitability and integration state.

Locomotor training improves reciprocal and nonreciprocal inhibitory control of soleus motoneurons in human spinal cord injury

“…We have recently shown that locomotor training changes the behavior of short-and long-latency flexion reflexes, reestablishes a physiologic soleus H-reflex phasedependent modulation, increases presynaptic inhibitory control of soleus motoneurons, modifies excitability properties of so- percentage of change of the conditioned H reflex during seated from all subjects after training, reflecting the magnitude of reciprocal and nonreciprocal inhibition, is plotted against the years postinjury. leus motoneurons, changes cocontraction levels between knee and ankle antagonistic muscles, and promotes interlimb and intralimb EMG coordination in the same people with SCI tested here (Knikou 2013;Knikou and Mummidisetty 2014;Smith et al 2014Smith et al , 2015. Because the modulation of soleus H-reflex inhibition by presynaptic inhibition after training was completely different from the soleus H-reflex postsynaptic inhibition in the same patients tested in this study, the changes observed after locomotor training can be attributed to changes in the intrinsic properties, function, and synaptic inputs of Ia and Ib inhibitory interneurons.…”

“…Subjects' consent was obtained according to the Declaration of Helsinki. Subjects also participated in previous studies (Knikou 2013;Knikou and Mummidisetty 2014;Smith et al 2014Smith et al , 2015 and are identified here with the same code. Subjects R09 and R20 did not participate in the Ib inhibition experiment.…”

“…We have recently shown that locomotor training induces plastic changes of flexor and extensor reflexes, presynaptic inhibition of soleus Ia afferents, and soleus H-reflex habituation at rest and during stepping in individuals with SCI (Knikou 2013;Knikou and Mummidisetty 2014;Smith et al 2014Smith et al , 2015. Most notable is the reemergence of the soleus H-reflex phase-dependent modulation (Knikou 2013), which can be viewed as a net plasticity of multiple spinal neuronal circuits.…”

Supraspinal Control Predicts Locomotor Function and Forecasts Responsiveness to Training after Spinal Cord Injury

“…71 Persons with SCI who participate in locomotor training demonstrate more typical modulation of spinal reflex excitability after training compared with their pre-training levels. [72][73][74][75] The importance of changes in reflexes should be considered in conjunction with observable improvements in overground walking; for example, improvement in overground walking speed is correlated with reduction in clonus and H-reflex magnitude. 73,76 The observation that reflex modulation can change in the absence of measurable change in the walking outcome, 77 however, suggests either that the reflex modulation is an epiphenomenon unrelated to walking performance or that the walking measures are not sufficiently sensitive to the changes in gait that accompany improved reflex modulation.…”

Stretching adversely modulates locomotor capacity following spinal cord injury via activation of nociceptive afferents.

“…However, existing evidence suggests that transmission of nociceptive signals results in a multitude of unfavorable effects over the locomotor circuitry [212,213] that has an otherwise high capacity for retraining, given the appropriate proprioceptive feedback [153,[214][215][216].…”