Task-specificity vs. ceiling effect: step-training in shallow water after spinal cord injury

Abstract

While activity-based rehabilitation is one of the most promising therapeutic approaches for spinal cord injury, the necessary components for optimal locomotor retraining have not yet been determined. Currently, a number of different activity-based approaches are being investigated including body weight-supported treadmill training (with and without manual assistance), robotically-assisted treadmill training, bicycling and swimming, among others. We recently showed, in the adult rat, that intensive rehabilitation based on swimming brought about significant improvements in hindlimb performance during swimming but did not alter the normal course of recovery of over-ground walking (Smith et al., 2006a,b, 2009). However, swimming lacks the phasic limb-loading and plantar cutaneous feedback thought to be important for weight-supported step training. So, we are investigating an innovative approach based on walking in shallow water where buoyancy provides some body weight support and balance while still allowing for limb-loading and appropriate cutaneous afferent feedback during retraining. Thus, the aim of this study is to determine if spinal cord injured animals show improved overground locomotion following intensive body weight-supported locomotor training in shallow water. The results show that training in shallow water successfully improved stepping in shallow water, but was not able to bring about significant improvements in overground locomotion despite the fact that the shallow water provides sufficient body weight support to allow acutely injured rats to generate frequent plantar stepping. These observations support previous suggestions that incompletely injured animals retrain themselves while moving about in their cages and that daily training regimes are not able to improve upon this already substantial functional improvement due to a ceiling effect, rather than task-specificity, per se. These results also support the concept that moderately-severe thoracic contusion injuries decrease the capacity for body weight support, but do not decrease the capacity for pattern generation. In contrast, animals with severe contusion injuries could not support their body weight nor could they generate a locomotor pattern when provided with body weight support via buoyancy.

Figure 1

The BBB scores over time for 25 and 50g-cm injured animals are shown in A. Each outcome measure increased significantly from week 1 to week 3 (ANOVA and post-hoc t-test; *, p<.01; **, p<.05). The inset shows the mean spared white matter (SWM; cross sectional area) at the injury epicenter, which was significantly different for the two groups (Independent t-test; *, p<.05). B. The angular excursion of the IHA (iliac crest – hip – ankle) and HAT (hip – ankle – toe) angles over time are shown for 3 steps taken by a representative 25g-cm injured rat at week 1 with the weight support of 5cm of water. C shows the mean PSI ± SD (Plantar Stepping Index) for 25g-cm injured animals at weeks 1, 2 and 3 when assessed walking in a dry tank (Dry) and with the weight support of 5cm of water (Wet). Animals achieved significantly higher PSIs when walking in 5cm of water as compared to a dry tank at each time point tested (Independent t-test; *, p<.05). D. Shown is the mean PSI ± SD for 50g-cm injured animals at weeks 1, 2 and 3 assessed in both the dry and wet (5cm of water) conditions. The PSI indicates that these animals could achieve a few plantar hindlimb steps in 5cm of water but could not when walking in a dry tank.

Figure 2

The results from the phase 2 experiment are shown in A and B as the BBB scores over time for 25 (A) and 50g-cm (B) injured groups that received training in shallow water (black squares) or remained untrained (red diamonds). Training had no significant effect on BBB scores (repeated measures ANOVA). Insets show that the mean spared white matter (cross sectional area) at the injury epicenter was not different for the trained and untrained groups for each injury severity. C shows that 25g-cm injured animals that were trained in shallow water achieved a significantly higher mean PSI when stepping in shallow water than when stepping in a dry tank (Independent t-test; *, p<.05) and a significantly higher mean PSI than the untrained group stepping in a dry tank or in shallow water (Independent t-test; **, p<.05). In contrast, training had no influence on the mean PSI of the trained and untrained 50g-cm injured animals. Still images taken from sagittal and ventral video of 25g-cm injured animals stepping in shallow water are shown in D to illustrate the limb positions during plantar stepping from both aspects (means ± SD).

Figure 3

The graph shown in A compares the mean peak (extension), trough (flexion) and excursion of the hip-ankle-toe angle for trained and untrained 25g-cm injured animals, in both dry and wet (5cm of water) conditions, with uninjured baseline measures (normal, dry) at 9 weeks post-injury after 8 weeks of training (all are means ± SD). No group differences were detected except for the untrained group that had a significantly higher mean peak (extension) in the dry tank compared to baseline (normal, dry; Independent t-test; *, p<.05). The stick figures in B and C illustrate the limb and joint movements during stepping of a representative trained 25g-cm injured animal in shallow water (B) and in a dry tank (C). In shallow water the point representing the toe remains fixed during stance. In contrast, when walking in a dry tank this animal exhibited dragging of the hindlimb in both extended and flexed states as illustrated by the movement of the point representing the toe relative to the bottom of the tank (contact).

Figure 4

In A, the mean BBB scores (± SD) of trained and untrained 25g-cm injured animals are shown over time relative to the depth of water utilized during training sessions occurring the week of the assessment. No group differences were found at any time point. The inset shows the spared white matter at the injury epicenter for the two experimental groups, which were not different. In B, still images taken from digital videos of the ventral view of the same trained 25g-cm injured animal show the placement of fore and hindpaws during stepping in shallow water (top) and in a dry tank (bottom). Orange arrows designate dragging of the hindlimb with the ankle in an extended position (dorsal contact) and red arrows designate dragging of the hindlimb with the ankle in a flexed position (plantar contact).

Figure 5

Shown in A are the means ± SD for the peak (extension), trough (flexion) and excursion of the hip, knee and ankle of trained and untrained 25g-cm injured animals, pre-injury (baseline), at week 1 post-injury (pre-retraining) and at week 9, after 8 weeks of training or cage rest (untrained). Asterisks (*) indicate significant differences from baseline for maximum joint extension (peak, top of bar), maximum joint flexion (trough, bottom of bar) and total joint excursion (peak - trough, middle of bar). These data were analyzed using repeated-measures ANOVA followed by a Tukey's post-hoc t-test. With the exception of ankle excursion, no significant differences were found for trained or untrained groups compared to baseline measures or for the trained group compared to the untrained group. B. The mean PSI and RI (± SD) for walking in a dry tank were not statistically different for trained compared to untrained animals. The stick figures shown in C represent three common occurrences observed during stepping in a dry tank: 1. Plantar drag (when the plantar surface of the paw is visible to the ventral camera and is in contact with the surface but is dragged along the surface without providing significant weight support). This is not defined as a plantar step for the PSI. 2. Plantar step (where the plantar surface of the paw is clearly visible to the camera and does not shift position until swing is initiated). This kind of step is associated with weight support as reflected by the hip height and would be defined as a plantar step for the PSI. 3. A limb drag with the ankle extended (the plantar surface of the paw is not visible to the ventral camera and the hip height is low). This would not be defined as a plantar step for the PSI.