Increased spinal reflex excitability is associated with enhanced central activation during voluntary lengthening contractions in human spinal cord injury

Abstract

This study of chronic incomplete spinal cord injury (SCI) subjects investigated patterns of central motor drive (i.e., central activation) of the plantar flexors using interpolated twitches, and modulation of soleus H-reflexes during lengthening, isometric, and shortening muscle actions. In a recent study of the knee extensors, SCI subjects demonstrated greater central activation ratio (CAR) values during lengthening (i.e., eccentric) maximal voluntary contractions (MVCs), compared with during isometric or shortening (i.e., concentric) MVCs. In contrast, healthy controls demonstrated lower lengthening CAR values compared with their isometric and shortening CARs. For the present investigation, we hypothesized SCI subjects would again produce their highest CAR values during lengthening MVCs, and that these increases in central activation were partially attributable to greater efficacy of Ia-α motoneuron transmission during muscle lengthening following SCI. Results show SCI subjects produced higher CAR values during lengthening vs. isometric or shortening MVCs (all P < 0.001). H-reflex testing revealed normalized H-reflexes (maximal SOL H-reflex-to-maximal M-wave ratios) were greater for SCI than controls during passive (P = 0.023) and active (i.e., 75% MVC; P = 0.017) lengthening, suggesting facilitation of Ia transmission post-SCI. Additionally, measures of spinal reflex excitability (passive lengthening maximal SOL H-reflex-to-maximal M-wave ratio) in SCI were positively correlated with soleus electromyographic activity and CAR values during lengthening MVCs (both P < 0.05). The present study presents evidence that patterns of dynamic muscle activation are altered following SCI, and that greater central activation during lengthening contractions is partly due to enhanced efficacy of Ia-α motoneuron transmission.

Keywords: H-reflex; central activation ratio; eccentric contractions; spinal cord injury.

Fig. 1.

Representative data during plantar flexor (PF) maximal voluntary contractions (MVCs). Comparison of central activation patterns between representative healthy control (A) and spinal cord injury (SCI) (B) subjects is shown. A: the healthy control subject shows near maximal central activation across all contraction types (i.e., small evoked twitch). B: the SCI subject demonstrates overall deficits in central activation across contraction types, but generates greater volitional torque and soleus (SOL) electromyogram (EMG) during lengthening MVCs. TA, tibialis anterior.

Fig. 2.

Evoked twitches and group data from central activation ratio (CAR) trials. A: isolated evoked twitches from the SCI subject's MVC trials in Fig. 1B. Smallest evoked twitch was observed during the lengthening MVC. B: SCI subjects demonstrate overall deficits in central activation, but generate greater central activation during lengthening MVCs than during isometric or shortening MVCs. C: group comparisons of normalized SOL EMG values reveal SCI subjects generate increases in SOL muscle activity during lengthening MVCs compared with isometric or shortening MVCs. Normalized SOL values for SCI subjects were also ∼45% greater than that of controls during lengthening MVCs. D: SCI subjects demonstrated greater coactivation of the antagonist TA muscle than controls during PF MVCs (P < 0.05). However, no differences in TA activity across contraction types were observed in either group (P > 0.05). DF, dorsiflexor; MVIC, maximum volitional isometric contraction. Values are means ± SE. Asterisks not associated with brackets refer to significant between groups differences (i.e., SCI vs. control). **P < 0.01. ***P < 0.001.

Fig. 3.

Passive H-reflexes. A: the representative control subject demonstrates a strong depression of maximal SOL H-reflex (Hmax) amplitudes during passive muscle lengthening actions. B: there is less inhibition of Hmax during passive lengthening in the SCI subject compared with the control. C: group data for Hmax-to-maximal M-wave (Mmax) ratios (Hmax/Mmax) reveal SCI subjects produce significantly higher Hmax/Mmax during passive muscle lengthening than controls. Values are means ± SE. *P < 0.05. **P < 0.01. ***P < 0.001.

Fig. 4.

H-reflexes during 75% MVC contractions. A: during strong contractions, there is potentiation of H-reflexes, but specific depression of lengthening H-reflexes is still demonstrated by the control subject. B: there is a complete disinhibition of the lengthening H-reflex in this representative SCI subject. C: during voluntary contractions, SCI subjects continue to demonstrate a larger Hmax/Mmax than controls. In addition, there are no longer any differences in Hmax/Mmax across contraction types for the SCI group, whereas there is still depression of lengthening Hmax/Mmax for controls. Values are means ± SE. *P < 0.05. ***P < 0.001.

Fig. 5.

Correlations in SCI subjects between spinal reflex excitability during passive muscle lengthening and central activation during lengthening MVCs. A: there is a significant positive correlation between passive lengthening Hmax/Mmax and SOL EMG during lengthening MVCs in SCI subjects when both are expressed as percentages of their corresponding isometric values. B: similarly, a significant positive correlation exists between lengthening Hmax/Mmax and lengthening CAR values.