Treadmill training enhances the recovery of normal stepping patterns in spinal cord contused rats

Abstract

Treadmill training is known to improve stepping in complete spinal cord injured animals. Few studies have examined whether treadmill training also enhances locomotor recovery in animals following incomplete spinal cord injuries. In the present study, we compared locomotor recovery in trained and untrained rats that received a severe mid-thoracic contusion of the spinal cord. A robotic device was used to train and to test bipedal hindlimb stepping on a treadmill. Training was imposed for 8 weeks. The robotic device supported the weight of the rats and recorded ankle movements in the hindlimbs for movement analyses. Both the trained and untrained rats generated partial weight bearing hindlimb steps after the spinal cord contusion. Dragging during swing was more prevalent in the untrained rats than the trained rats. In addition, only the trained rats performed step cycle trajectories that were similar to normal step cycle trajectories in terms of the trajectory shape and movement velocity characteristics. In contrast, untrained rats executed step cycles that consisted of fast, kick-like movements during forward swing. These findings indicate that spinal cord contused rats can generate partial weight bearing stepping in the absence of treadmill training. The findings also suggest that the effect of treadmill training is to restore normal patterns of hindlimb movements following severe incomplete spinal cord injury in rats.

Fig. 1

Examples of stepping movements recorded by the robotic device in an untrained rat 14 weeks after a spinal contusion. (A) The horizontal (thin lines) and vertical (thick lines) displacement of the ankle is shown. The “s” indicate successful partial weight bearing steps with lift of the hindpaw whereas the “d” indicates steps with paw dragging. (B) The trajectory of the ankle during a single step cycle from one spinally contused rat. For movement analyses, the step cycle was divided into forward movement (black line with black squares) and backward movement (grey line with grey squares). Arrows indicate the direction of movement. At 1, forward movement begins. 2 denotes the point in the trajectory that the ankle reached maximum height. At 3, forward movement ends and backward movement begins. 4 denotes the point in the trajectory that the ankle reached minimum height. At 5, backward movement ends.

Fig. 2

Number of steps executed by trained, untrained spinally contused rats and intact rats. The mean number of successful steps (A) and drag steps (B) performed by trained (black squares) and untrained (white diamonds) rats 6 weeks and 14 weeks after spinal contusion are shown. Data from intact animals (black triangle) are also shown. Successful steps are defined as steps in which the paw was lifted during swing (see “s” in Fig. 1A). Drag steps are steps in which the paw dragged during swing (see “d” in Fig. 1A). In (C), the percentage of drag steps relative to the total number of stepping movements is shown. All of the data in Fig. 2 are partial weight bearing steps with 85% of the body weight supported by the robotic device. The average ± standard error is shown (n = 13 trained rats; n = 13 untrained rat; n = 9 intact rats). * indicates significant difference between untrained and trained (p ≤ 0.01), # indicates significant difference between untrained and normal (p ≤ 0.01) and † indicates significant difference between Week 14 and week 6.

Fig. 3

Average step cycle trajectories in (A) untrained and (B) trained spinally contused rats and (C) intact rats. Forward and backward movements are indicated by the black and white lines respectively. Arrows and the numbers (1–5) indicate the direction and progression of movement (see Fig. 1 for details). The trajectories shown are group averages. Grey areas around the mean trajectory indicate standard error. Only the trajectories from rats that performed at least 15 steps were included in these averages (n = 9 untrained; n = 8 trained; n = 9 intact). The data from the contused rats are from tests performed 14 weeks after the contusion.

Fig. 4

Changes in the velocity during forward movement in untrained (thin black line), trained (thick grey line) and intact (thick black line) rats. Horizontal velocity is shown in (A) and vertical velocity is shown in (B). The changes in velocity are shown relative to the step cycle (the start of forward movement marks the beginning of the step cycle, 0%). Circles and vertical lines indicate the onset of the peak velocity during the step cycle. The data shown are group averages. Only the trajectories from rats that performed at least 15 steps were included in these averages (n = 9 untrained; n = 8 trained; n = 9 intact). The data from the contused rats are from tests performed 14 weeks after the contusion. *† indicates that the onset of the peak velocity is significantly earlier than the onset of the peak velocity in the trained (p < 0.05) and normal rats respectively (p ≤ 0.01).

Fig. 5

Plot of horizontal versus vertical velocity of the ankle during forward movement in (A) untrained, (B) trained and (C) intact rats. Arrows indicate the direction of movement. The velocity data shown are group averages. Only the trajectories from rats that performed at least 15 steps were included in these averages (n = 9 untrained; n = 8 trained; n = 9 intact). The data from the contused rats are from tests performed 14 weeks after the contusion.

Fig. 6

Changes in the velocity during backward movement in (A) untrained, (B) trained and (C) intact rats. Horizontal velocity (grey line) and vertical velocity is shown (black line). The changes in velocity are shown relative to the step cycle (backward movements began after 10% of the step cycle had been completed). The white squares indicate the mean onset of the peak horizontal velocity during the step cycle. The bars around the white squares indicate the standard error of the mean onset. The data shown are group averages. Only the trajectories from rats that performed at least 15 steps were included in these averages (n = 9 untrained; n = 8 trained; n = 9 intact). The data from the contused rats are from tests performed 14 weeks after the contusion. *† indicates that the onset of the peak velocity is significantly earlier than the onset of the peak velocity in the trained and normal rats respectively (p ≤ 0.01).