1. Neuroscience
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The recovery of standing and locomotion after spinal cord injury does not require task-specific training

  1. Jonathan Harnie
  2. Adam Doelman
  3. Emmanuelle de Vette
  4. Johannie Audet
  5. Etienne Desrochers
  6. Nathaly Gaudreault
  7. Alain Frigon  Is a corresponding author
  1. Université de Sherbrooke, Centre de Recherche du CHUS, Canada
Research Article
Cite this article as: eLife 2019;8:e50134 doi: 10.7554/eLife.50134
7 figures, 9 videos, 1 table and 2 additional files

Figures

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.

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.

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.

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.

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.

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.

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.

Videos

Video 1
Standing performance scale.

The video shows the rating of standing performance on a six-point scale, from 0 to 5.

Video 2
Recovery of full weight bearing standing without perineal stimulation two weeks after spinal transection.

The video shows the recovery of full weight bearing standing two weeks after spinal transection in three cats, one from each experimental group.

Video 3
Some cats did not recover the capacity to stand after spinal transection.

The video shows an example of a cat (Cat 7) that did not recover standing five weeks after spinal transection without perineal stimulation.

Video 4
The effects of perineal stimulation on standing five weeks after spinal transection.

The video shows three examples of the effects of stimulating the perineal region after spinal transection five weeks after spinal transection in three cats. (A) Perineal stimulation restored weight bearing during standing. (B) In a cat that had weight bearing during standing, perineal stimulation slightly elevated the pelvis by extending the hindlimbs. (C) In a cat that had weight bearing during standing, perineal stimulation generated stomping in place.

Video 5
Recovery of full weight bearing hindlimb locomotion six weeks after spinal transection.

The video shows the recovery of full weight bearing hindlimb locomotion without perineal stimulation six weeks after spinal transection at a treadmill speed of 0.4 m/s in three cats, one from each experimental group.

Video 6
Some cats did not recover hindlimb locomotion after spinal transection.

The video shows an example of a cat (Cat 7) from the Locomotor-trained group that did not recover hindlimb locomotion without perineal stimulation six weeks after spinal transection. The treadmill speed was set at 0.4 m/s.

Video 7
The effects of perineal stimulation on hindlimb locomotion six weeks after spinal transection.

The video shows the effects of perineal stimulation on four cats, one from Groups 1 (Non-specific) and 3 (Untrained) and two from Group 2 (Locomotor-trained), on hindlimb locomotion at a treadmill speed of 0.4 m/s six weeks after spinal transection. Left and right panels respectively show hindlimb locomotion without and with perineal stimulation.

Video 8
Speed modulation during locomotion recovers without specific training six weeks after spinal transection.

The video shows hindlimb locomotion at treadmill speeds of 0.4 m/s (left panel) and 1.0 m/s (right panel) in three cats, one from each experimental group, six weeks after spinal transection with perineal stimulation.

Video 9
The capacity for split-belt locomotion recovers without specific training six weeks after spinal transection.

The video shows the hindlimb locomotor pattern on a split-belt treadmill in three cats, one from each experimental group, six weeks after spinal transection with (Cat 2 and Cat 5) or without (Cat 9) perineal stimulation. For each cat, the slow belt operated at a speed of 0.4 m/s while the fast belt was set at 0.5 m/s (left panel) and 1.0 m/s (right panel).

Tables

Table 1
Locomotor performance of individual cats six weeks post-transection without and with perineal stimulation.

Individual cats are listed on the left along with the group (G) they belonged to and whether they were female (F) or male (M). The table shows several locomotor parameters for individual cats of the three groups, including the maximal speed during tied-belt locomotion, tested up to 1.0 m/s, and the maximal speed of the fast limb during split-belt locomotion. For split-belt locomotion, the slow limb stepped at 0.4 m/s while the left (L) and right (R) hindlimbs were tested up to a maximal speed of 1.0 m/s. NT, Not tested; Y, proper digitigrade placement of the paw at contact; I, inconsistent paw placement. A dash mark indicates an inability to perform hindlimb locomotion.

Without perineal stimulationWith perineal stimulation
CatMaximal speed (m/s)
Tied-belt
Maximal speed (m/s)
Split-belt
# of consecutive stepsProper
Paw placement
Maximal speed (m/s)
Tied-belt
Maximal speed (m/s)
Split-belt
# of consecutive stepsProper
Paw placement
1-G1 (F)1.0L: 1.0; R: 1.0>10Y1.0L: 1.0; R: 1.0>10Y
2-G1 (F)0.4-NTNT>10Y1.0L: 1.0; R: 1.0>10Y
3-G1 (M)0.0///1.0L: 1.0; R: 1.0<10I
4-G1 (M)0.4-NTNT>10Y1.0L: 1.0; R: 1.0>10Y
5-G2 (F)1.0L:0.7; R: 1.0>10Y1.0L: 1.0; R: 1.0>10Y
6-G2 (F)1.0L: 1.0; R: 1.0>10Y0.8NT>10Y
7-G2 (F)0.0///0.0///
8-G2 (M)0.0///0.0///
9-G3 (F)1.0L: 0.7; R: 1.0>10Y1.0L: 1.0; R: 1.0>10Y
10-G3 (F)1.0L: 0.8; R: 0.8>10Y1.0L: 0.8; R: 0.8>10Y
11-G3 (M)0.0///1.0L: 1.0; R: 1.0>10I
12-G3 (M)0.4-NTNT<10I1.0L: 0.9; R: 0.9>10I

Data availability

Source data for the figures can be found in Source data 1.

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