Locomotor training modifies soleus monosynaptic motoneuron responses in human spinal cord injury

Abstract

The objective of this study was to assess changes in monosynaptic motoneuron responses to stimulation of Ia afferents after locomotor training in individuals with chronic spinal cord injury (SCI). We hypothesized that locomotor training modifies the amplitude of the soleus monosynaptic motoneuron responses in a body position-dependent manner. Fifteen individuals with chronic clinical motor complete or incomplete SCI received an average of 45 locomotor training sessions. The soleus H-reflex and M-wave recruitment curves were assembled using data collected in both the right and left legs, with subjects seated and standing, before and after training. The soleus H-reflexes and M-waves, measured as peak-to-peak amplitudes, were normalized to the maximal M-wave (M(max)). Stimulation intensities were normalized to 50% M(max) stimulus intensity. A sigmoid function was also fitted to the normalized soleus H-reflexes on the ascending limb of the recruitment curve. After training, soleus H-reflex excitability was increased in both legs in AIS C subjects, and remained unchanged in AIS A-B and AIS D subjects during standing. When subjects were seated, soleus H-reflex excitability was decreased after training in many AIS C and D subjects. Changes in reflex excitability coincided with changes in stimulation intensities at H-threshold, 50% maximal H-reflex, and at maximal H-reflex, while an interaction between leg side and AIS scale for the H-reflex slope was also found. Adaptations of the intrinsic properties of soleus motoneurons and Ia afferents, the excitability profile of the soleus motoneuron pool, oligosynaptic inputs, and corticospinal inputs may all contribute to these changes. The findings of this study demonstrate that locomotor training impacts the amplitude of the monosynaptic motoneuron responses based on the demands of the motor task in people with chronic SCI.

Conflict of interest statement

Conflict of interest The authors have no conflicts of interest to report.

Figures

Fig. 1

Soleus H-reflex and M-wave recruitment curves before and after locomotor training in the right leg during standing grouped separately for AIS A-B, AIS C, and AIS D subjects. a–c Mean M-wave sizes as a percentage of the maximal M-wave are plotted in multiples of 50 % of Mmax stimulus intensity. d–f Mean soleus H-reflex sizes as a percentage of the maximal M-wave are plotted in multiples of 50 % of Mmax stimulus intensity. g–i Sigmoid input–output relation for soleus H-reflexes elicited on the ascending portion of the recruitment curve. The P values for graphs a–c are the results of the oneway ANOVAs conducted on the normalized M-waves from the start until the end of the recruitment curve before and after training. The P values for graphs d–e are the results of the two-way ANOVAs conducted on the normalized H-reflexes on the ascending portion of the H-reflex recruitment curve as a function of stimulus intensity and time of testing

Fig. 2

Soleus H-reflex and M-wave recruitment curves before and after locomotor training in the left leg during standing grouped separately for AIS B, AIS C, and AIS D subjects. a–c Mean M-wave sizes as a percentage of the maximal M-wave are plotted in multiples of 50 % of Mmax stimulus intensity. d–f Mean soleus H-reflex sizes as a percentage of the maximal M-wave are plotted in multiples of 50 % of Mmax stimulus intensity. g–i Sigmoid input–output relation for soleus H-reflexes elicited on the ascending part of the recruitment curve. The P values for graphs a–c are the results of the one-way ANOVAs conducted on the normalized M-waves from the start until the end of the recruitment curve before and after training. The P values for graphs d–e are the results of the two-way ANOVAs conducted on the normalized H-reflexes on the ascending portion of the H-reflex recruitment curve as a function of stimulus intensity and time of testing

Fig. 3

Soleus H-reflex and M-wave recruitment curves before and after locomotor training in the right leg during seated grouped separately for AIS B, AIS C, and AIS D subjects. a–c Mean M-wave sizes as a percentage of the maximal M-wave are plotted in multiples of 50 % of Mmax stimulus intensity. d–f Mean soleus H-reflex sizes as a percentage of the maximal M-wave are plotted in multiples of 50 % of Mmax stimulus intensity. g–i Sigmoid input–output relation for soleus H-reflexes elicited on the ascending part of the recruitment curve. The P values for graphs a–c are the results of the one-way ANOVAs conducted on the normalized M-waves from the start until the end of the recruitment curve before and after training. The P values for graphs d–e are the results of the two-way ANOVAs conducted on the normalized H-reflexes on the ascending portion of the H-reflex recruitment curve as a function of stimulus intensity and time of testing

Fig. 4

Soleus H-reflex and M-wave recruitment curves before and after locomotor training in the left leg during seated grouped separately for AIS A-B, AIS C, and AIS D subjects. a–c Mean M-wave sizes as a percentage of the maximal M-wave are plotted in multiples of 50 % of Mmax stimulus intensity. d–f Mean soleus H-reflex sizes as a percentage of the maximal M-wave are plotted in multiples of 50 % of Mmax stimulus intensity. g–i Sigmoid input–output relation for soleus H-reflexes elicited on the ascending part of the recruitment curve. The P values for graphs a–c are the results of the one-way ANOVAs conducted on the normalized M-waves from the start until the end of the recruitment curve before and after training. The P values for graphs d–e are the results of the two-way ANOVAs conducted on the normalized H-reflexes on the ascending portion of the H-reflex recruitment curve as a function of stimulus intensity and time of testing

Fig. 5

Background EMG activity. a Normalized soleus background EMG activity. b Modulation indices of soleus background EMG activity. c Background soleus/tibialis anterior ratio. Overall mean ± SEM from all SCI subjects before and after training for the right and left leg during seated and standing