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The Recovery of Standing and Locomotion After Spinal Cord Injury Does Not Require Task-Specific Training

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The Recovery of Standing and Locomotion After Spinal Cord Injury Does Not Require Task-Specific Training

Jonathan Harnie et al. Elife.

Abstract

After complete spinal cord injury, mammals, including mice, rats and cats, recover hindlimb locomotion with treadmill training. The premise is that sensory cues consistent with locomotion reorganize spinal sensorimotor circuits. Here, we show that hindlimb standing and locomotion recover after spinal transection in cats without task-specific training. Spinal-transected cats recovered full weight bearing standing and locomotion after five weeks of rhythmic manual stimulation of triceps surae muscles (non-specific training) and without any intervention. Moreover, cats modulated locomotor speed and performed split-belt locomotion six weeks after spinal transection, functions that were not trained or tested in the weeks prior. This indicates that spinal networks controlling standing and locomotion and their interactions with sensory feedback from the limbs remain largely intact after complete spinal cord injury. We conclude that standing and locomotor recovery is due to the return of neuronal excitability within spinal sensorimotor circuits that do not require task-specific activity-dependent plasticity.

Keywords: Cat; Felis catus; central pattern generator; functional recovery; locomotor training; neuroscience; spinal cord injury; task-specificity.

Conflict of interest statement

JH, AD, Ed, JA, ED, NG, AF No competing interests declared

Figures

Figure 1.
Figure 1.. Schematic representation of experimental timeline and set-ups.
(A) Timeline of experiments. After transection, we performed stand and locomotor testing each week (W1–W5) in 9 of 12 cats and locomotor testing in all cats at W6. (B) Experimental set-ups for the application of manual therapy (left panel) and for locomotor testing/training (right panel). (C) Histological analysis of spinal lesion site.
Figure 2.
Figure 2.. Recovery of weight bearing during standing after spinal transection.
(A) Weight bearing during standing performance at weeks 1 to 5 (W1–W5) after spinal transection in nine individual cats without and with perineal stimulation using a 6-point scale (right panels). (B) Electromyography (EMG) of the right (R) and left (L) soleus (SOL) and tibialis anterior (TA) muscles without and with perineal stimulation (gray area) in three cats during standing five weeks after spinal transection. (C) Effect of perineal stimulation on the mean EMG amplitude of SOL and TA at weeks 1 to 5 after spinal transection of 9 individual cats obtained during 1 s of weight bearing with perineal stimulation expressed as a percentage of the amplitude obtained without perineal stimulation. P values from paired t-tests are indicated above the data points. *, p<0.05; **, p<0.01; ***, p<0.001.
Figure 3.
Figure 3.. Recovery of hindlimb locomotion after spinal transection.
(A) Hindlimb locomotor performance during tied-belt locomotion at 0.4 m/s at weeks 1 to 6 (W1–W6) after spinal transection in nine (W1–W5) and twelve (W6) individual cats without and with perineal stimulation using a nine-point scale. (B) A stick figure diagram of a representative cycle showing kinematics of the right hindlimb without and with perineal stimulation before (Intact) and six weeks after spinal transection during tied-belt locomotion at 0.4 m/s in the twelve cats. Gray areas indicate animals that could not step.
Figure 4.
Figure 4.. Hindlimb muscle activity during locomotion before and after spinal transection.
(A) Hindlimb locomotor pattern before (Intact) and six weeks after transection in four cats from the three groups, including two from Group 2, during tied-belt locomotion at 0.4 m/s. The effects of perineal stimulation is shown after spinal transection. Each panel shows the EMG from four hindlimb muscles from the right (R) and left (L) hindlimbs: SOL, soleus; BFA, biceps femoris anterior; SRT, anterior sartorius. (B) Cycle, stance and swing durations and the phasing between hindlimbs with no (NPS) or with (PS) perineal stimulation at 6 weeks after spinal transection. (C) Effect of perineal stimulation on the burst durations and mean EMG amplitudes of the triceps surae (TS, soleus n = 8 or lateral gastrocnemius n = 2) or SRT (n = 7) muscles at 6 weeks after spinal transection. P values above panels in B and C from paired t-tests comparing values obtained without and with perineal stimulation.
Figure 5.
Figure 5.. Speed modulation during tied-belt locomotion before and six weeks after spinal transection.
(A) Hindlimb locomotor pattern before (Intact) and six weeks after spinal transection in three cats, one from each group, during tied-belt locomotion at 0.4 m/s and at 1.0 m/s in the spinal state. In the examples shown, cats stepped with perineal stimulation. Each panel shows the EMG from four hindlimb muscles from the right (R) and left (L) hindlimbs: BFA, biceps femoris anterior; SRT, anterior sartorius; VL, vastus lateralis. (B) Cycle, stance and swing durations and the phasing between hindlimbs. All cats stepped with perineal stimulation except for Cat 6. Each data point is the mean of 10–15 cycles.
Figure 6.
Figure 6.. Modulation of muscle activity with increasing treadmill speed during tied-belt locomotion six weeks after spinal transection.
From the top, the first panel shows burst durations of the vastus lateralis (VL, n = 4) or biceps femoris anterior (BFA, n = 6) muscles while the second panel shows burst durations of the anterior sartorius (SRT, n = 9) muscle for individual cats, separated by group, as a function of treadmill speed. The third and fourth panels show the mean EMG amplitudes of the VL-BFA and SRT, respectively, for individual cats, separated by group, as a function of treadmill speed. All cats stepped with perineal stimulation except for Cat 6. Each data point is the mean of 10–15 cycles.
Figure 7.
Figure 7.. Split-belt locomotion six weeks after spinal transection.
(A) Hindlimb locomotor pattern six weeks after spinal transection in three cats, one from each group during split-belt locomotion with the slow (left) hindlimb stepping at 0.4 m/s and the fast (right) hindlimb stepping at 0.5 m/s, 0.7 m/s and at 1.0 m/s. In the examples shown, Cat 2 and Cat 5 stepped with perineal stimulation while Cat 9 stepped without. Each panel shows the EMG from 4 hindlimb muscles from the right (R) and left (L) hindlimbs: BFA, biceps femoris anterior; SRT, anterior sartorius; VL, vastus lateralis. (B) Cycle, stance and swing durations and the phasing between hindlimbs for the fast (left panels) and slow (right panels) limbs. All cats stepped with perineal stimulation except for Cats 6, 9 and 10. Each data point is the mean of 10–15 cycles. Note, that some intermediate speeds were not tested in Cat 11.

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