Operant conditioning of a spinal reflex can improve locomotion after spinal cord injury in humans

Abstract

Operant conditioning protocols can modify the activity of specific spinal cord pathways and can thereby affect behaviors that use these pathways. To explore the therapeutic application of these protocols, we studied the impact of down-conditioning the soleus H-reflex in people with impaired locomotion caused by chronic incomplete spinal cord injury. After a baseline period in which soleus H-reflex size was measured and locomotion was assessed, subjects completed either 30 H-reflex down-conditioning sessions (DC subjects) or 30 sessions in which the H-reflex was simply measured [unconditioned (UC) subjects], and locomotion was reassessed. Over the 30 sessions, the soleus H-reflex decreased in two-thirds of the DC subjects (a success rate similar to that in normal subjects) and remained smaller several months later. In these subjects, locomotion became faster and more symmetrical, and the modulation of EMG activity across the step cycle increased bilaterally. Furthermore, beginning about halfway through the conditioning sessions, all of these subjects commented spontaneously that they were walking faster and farther in their daily lives, and several noted less clonus, easier stepping, and/or other improvements. The H-reflex did not decrease in the other DC subjects or in any of the UC subjects; and their locomotion did not improve. These results suggest that reflex-conditioning protocols can enhance recovery of function after incomplete spinal cord injuries and possibly in other disorders as well. Because they are able to target specific spinal pathways, these protocols could be designed to address each individual's particular deficits, and might thereby complement other rehabilitation methods.

Figures

Figure 1.

A, Session schedule. Six baseline sessions were followed by 30 conditioning (DC subjects) or control (UC subjects) sessions, and then by two follow-up sessions. B, Composition of baseline, control, conditioning, and follow-up sessions. C, Visual feedback screens for control and conditioning trials (see text for full description).

Figure 2.

A, Final conditioned H-reflex sizes (i.e., average for the last three conditioning sessions) for individual DC and UC subjects. The data for normal DC subjects are from Thompson et al. (2009). The filled triangles represent the DC subjects whose conditioned H-reflexes for the last six conditioning sessions were significantly less than their H-reflexes for the six baseline sessions. The open triangles represent the DC subjects in whom the H-reflex did not decrease significantly. (The lowest open triangle failed to reach statistical significance due to high intersession variability.) B, C, Average conditioned (B) and control (C) H-reflexes for a baseline session (solid line) and the last conditioning session (dashed line) from a DC subject with SCI in whom the H-reflex decreased significantly. Both conditioned and control H-reflexes are smaller after 30 conditioning sessions. As summarized in Figure 3, A and B, the decrease in the control H-reflex is almost as great as that in the conditioned H-reflex. Background EMG and M-wave values do not change. A small stimulus artifact is present.

Figure 3.

A–F, Average (±SE) H-reflex values for baseline and conditioning sessions for DC subjects with SCI (A–C, N = 6; this study) and for normal subjects (D–F, N = 8; study by Thompson et al., 2009) in whom the H-reflex decreased significantly. A, D, Average conditioned H-reflex size. B, E, Average control H-reflex size. C, F, Average of conditioned H-reflex size minus control H-reflex size (i.e., task-dependent adaptation; see Results) (for details, see Thompson et al. (2009)). In the subjects with SCI, the conditioned H-reflex decreases to 69% of the baseline value over 30 conditioning sessions (A). This decrease consists of a relatively small task-dependent adaptation (−7%, C) and a relatively large across-session control reflex decrease (−24%, B). In the subjects without disability (Thompson et al., 2009), the conditioned H-reflex also decreases to 69% of the baseline value over 24 conditioning sessions (D). This decrease consists of a relatively large task-dependent adaptation (−15%, F) and a relatively small across-session control reflex decrease (−16%, E). The asterisks between B and E and between C and F indicate significant differences (p < 0.01) between subjects with SCI and normal subjects in final control H-reflex value and in task-dependent adaptation, respectively. Task-dependent adaptation is greater in the normal subjects, while change in the control H-reflex is greater in the subjects with SCI.

Figure 4.

A, Average (±SE) 10 m walking speeds after 30 conditioning or control sessions (in percentage of baseline speed) for subjects in whom the H-reflex did or did not decrease significantly. B, Step-cycle symmetry before (open bars) and after (shaded bars) 30 conditioning or control sessions for subjects in whom the H-reflex did or did not decrease significantly. Symmetry is measured as the ratio of the time between the nFC and the cFC (or simply stimulated, in the case of UC subjects) to the time between cFC and nFC. A ratio of 1 indicates a symmetrical gait. Initially, the ratio is >1. After the 30 conditioning or control sessions, the ratio has decreased toward 1 in the subjects in whom the H-reflex decreased, while it has increased in the subjects in whom the H-reflex did not decrease. C, Successive step cycles before and after conditioning from a subject in whom the H-reflex decreased. Each nFC (●) and cFC (○) are shown. The short vertical dashed lines mark the midpoints between nFCs (i.e., the midpoints of the step cycle), which is when cFC should occur. Before H-reflex down-conditioning, cFC occurs too late; after successful down-conditioning, it occurs on time.

Figure 5.

Rectified locomotor EMG activity in soleus, TA, VL, and BF muscles of both legs before (solid line) and after (dashed line) conditioning in a DC subject with SCI in whom the soleus H-reflex decreased. The step cycle is divided into 12 equal bins, starting from foot contact. Thus, bins 1–7 are for the stance phase and bins 8–12 are for the swing phase. After successful down-conditioning, EMG modulation over the step cycle is greater in both legs.

Figure 6.

Rectified soleus EMG and locomotor H-reflex size over the step cycle before and after H-reflex down-conditioning in a DC subject with SCI in whom the H-reflex decreased. The reduced spasticity after conditioning produces better soleus EMG modulation: the abnormal activity during the swing phase (arrows) is no longer present. In addition, the locomotor H-reflex is greatly decreased and better modulated after conditioning (i.e., it is lowest during the swing phase).

Figure 7.

Spontaneous comments made by subjects over the course of data collection. “X” indicates when a subject made the comment for the first time. Note that every subject in whom the H-reflex decreased reported walking faster and farther, and that these reports did not occur until substantial H-reflex decrease had occurred (i.e., Fig. 3).