44th SCI/D 

Symposium 2021‐04‐08

Restoring Locomotion by Arm

Cycling and Electrical
Stimulation after Spinal Cord
Injury
Vivian K. Mushahwar
Division of Physical Medicine and Rehabilitation
Department of Medicine and
Neuroscience and Mental Health Institute

Members of the SMART Network:

Multi-disciplinary and Multi-sector Stakeholders

Neuroscience, Engineering, Cell

Biology, Computer Science,
Magnetic Resonance, Medicine,
Rehabilitation, Health Economics,
Clinical Trials, Consumers

Restoring Function and Preventing Secondary

Complications

• Mobility (walking, arm function)

• Pressure Injuries • Deep vein thrombosis

Smart-e-Pants The SOCC

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44th SCI/D Symposium 2021‐04‐08

Activation of Spinal Networks:

• “Spinal cord center”

for locomotion

Picture from:
Dietz 2002

Micro-Implant in the Lumbosacral Enlargement to

Restore Walking after Paralysis

• “Spinal cord center”

for locomotion

Picture from:
Dietz 2002

Activation of Spinal Networks throughout

the Cord

Cartoon from:
Dietz 2002

Mushahwar, University of Alberta 2
44th SCI/D Symposium 2021‐04‐08

Activation of Spinal Networks throughout

the Cord

Arm swing neurally-driven: (Elftman,

1939; Fernandez-Ballesteros, 1965 …)

Arm movements modulate leg motor

output: (Kawashima; Zehr; Ferris;
Cartoon from:
Dietz 2002 Duysens; Dietz …)

Current strategies for the Rehabilitation of Walking

Behrman & Harkema, 2000 www.hocoma.com

The arms have not been involved actively and

systematically to improve walking

Activation of Spinal Networks throughout

the Cord

Would coordinated arm/leg

activation:
1) Improve walking capacity?
2) Enhance descending drive
to the legs?
3) Enhance (cervico-lumbar)
propriospinal modulation?
Cartoon from:
Dietz 2002

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44th SCI/D Symposium 2021‐04‐08

Cycling as an Efficient Intervention for

Improving Walking

• Coordinated activation
of the arms and leg

• Electrical stimulation for

assisting movement
generation

Zhou et al, 2018

10

Participants

A&L cycling (n=7) Leg cycling (n=8)

• 6 male, 1 female • 4 male, 4 female
• Age: 52 ± 7 year old • Age: 47 ± 11 year old

• AIS: C or D • AIS: C or D

• Level of injury: C3 to T12 • Level of injury: C4 to T10

• Years since injury: 9 ± 12 • Years since injury: 12 ± 14

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Training Protocol and Assessments:

Training:
• 1 hr/day, 5 days/week, 12
weeks
• Electrical stimulation applied to
the leg extensors

Assessments (no stim):

• Clinical
• Biomechanical
• Electrophysiological

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Mushahwar, University of Alberta 4
44th SCI/D Symposium 2021‐04‐08

Significant Improvements in Walking speed:

10 m walking test
Leg Pre-training: 0.50±0.08m/s A&L Pre-training: 0.45±0.08m/s
*
60
50% A&L
0.27 ± 0.072 m/s
Change in Walking
Speed (%)

40
*
0.092 ± 0.022 m/s
20
19% Leg

0
0 3 6 9 12
Training Time (weeks)
Zhou et al, 2018
13

Significant Improvements in Walking speed:

6 min walking test
Leg Pre-training: 157.1±20.3m A&L Pre-training: 164.5±22.6m
*
A&L
Change in Walking

40 37%
Distance (%)

26% Leg
20

0
0 3 6 9 12
Training Time (weeks)

Zhou et al, 2018

14

Results relative to Current Approaches:

Walking Speed

0.4 A&L
Change in walking
Speed (m/s)

0.3

0.2
Leg
0.1
52 43 35 64 19 20 8 7
0.0

Harkema 2012, >3yr iSCI Harkema 2012, 1-3yr iSCI

Alexeeva 2011 Field-Fote 2011
Yang 2011 Yang 2014
Leg Training A&L Training

Zhou et al, 2018

15

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44th SCI/D Symposium 2021‐04‐08

Results relative to Current Approaches:

Walking Speed

0.4 A&L
Change in walking
Speed (m/s)

0.3

0.2
Leg
0.1
52 43 35 64 19 20 8 7
0.0

Harkema 2012, >3yr iSCI Harkema 2012, 1-3yr iSCI

Alexeeva 2011 Field-Fote 2011
Yang 2011 Yang 2014
Leg Training A&L Training

Zhou et al, 2018

16

Our Results relative to Current Approaches:

Walking Distance

150
A&L
Change in walking
distance (meter)

100

Leg
50
64
52 43 20 8 7
0
Harkema 2012, >3yr iSCI(6-min)
Harkema 2012, 1-3yr iSCI(6-min)
Field-Fote 2011(2-min)
Yang 2014(6-min)

Zhou et al, 2018

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Regulation of Muscle Activation during Walking

Normalized EMG Amplitude (%)

100 NI TA average (n=6)

Onset of TA activation
80
Tibialis
Anterior Duration of TA activation
60

40

20

0
0 20 40 60 80 100
Gait Cycle (%)

http://naturalrunningcenter.com/wp-
content/uploads/2012/06/phases-of-gait-cycle1.jpg
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44th SCI/D Symposium 2021‐04‐08

Regulation of Muscle Activation during Walking

Normalized EMG Amplitude (%)

100 NI (n=6)
S3 (A&L)
pre-training
80 pre-training

60

40

20

0
0 20 40 60 80 100
Gait Cycle (%)

http://naturalrunningcenter.com/wp-
content/uploads/2012/06/phases-of-gait-cycle1.jpg
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Regulation of Muscle Activation during Walking

Normalized EMG Amplitude (%)

100 NI (n=6)
S3 (A&L) S3 (A&L)
pre-training
80 pre-training post-training
post-training
60

40

20
Muscle activation:
0
0 20 40 60 80 100 • onset of activation
Gait Cycle (%)
• duration of activation

http://naturalrunningcenter.com/wp-
content/uploads/2012/06/phases-of-gait-cycle1.jpg
20

Improvement in walking after Leg cycling

Pre-training: Post-training:
Pre-training: Post-training:

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44th SCI/D Symposium 2021‐04‐08

Improvement in walking after A&L cycling

Pre-training: Post-training:

• No weight-support
• Harness used for safety only

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Corticospinal excitability: Transcranial magnetic

stimulation (TMS), motor evoked potential (MEP)

magnetic
stimulation

cortex

MEP
spinal cord
silent period

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Example of MEP trace from one participant trace

1.2
1
Amplitude (mV)

0.8
0.6
0.4
0.2
0
-0.2
-0.4 Baseline activity Peak-to-peak MEP
-0.6

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Corticospinal drive: Tibialis Anterior Muscle

2.5 A&L Cycling

Amplitude of MEP (mV)

2
Pre-training
Post-training
Post-training
1.5

0.5
Pre-training
0
20 30 40 50 60 70 80 90

Stimulation intensity (%)

Zhou et al, 2017
25

Larger improvements in corticospinal drive after

A&L cycling than leg cycling

*
Change in TA MEP(max)

60
after training (%)

40 44.8%

20
19.4%

0
A&L
A&L Leg
 Leg
(n=7) (n=8)

Zhou et al, 2017

26

Propriospinal regulation: Effect of arm

movements on leg H-reflex

180°

270° 90°
• Activity-dependent?
(arms static vs. arms
0°
cycling)

Soleus
(SOL)
H-reflex

Zhou et al, 2018

27

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44th SCI/D Symposium 2021‐04‐08

Hoffman reflex (H-reflex)

1 Stim artifact
H-reflex 0.5

Amplitude (mV)
Ia afferent
0

Peripheral nerve ‐0.5

Background
‐1 muscle activity
α-motoneuron
M-Wave ‐1.5
M-wave
Peak-to-peak H-reflex

• Background muscle activity and motor response (M-wave)

maintained constant through out experiment

Trevor Barss
28
2021-04-08

Propriospinal regulation: Effect of arm

movements on leg H-reflex

180°

270° 90°
• Activity-dependent?
(arms static vs. arms
0°
cycling)

Soleus
(SOL)
H-reflex

Zhou et al, 2018

29

Effect of rhythmic arm cycling on Soleus

H-reflex:

4 cycling
Arms static
(mV)
H-reflex (mV)

Arms static
H-reflex
2 Stim artifact
Soleus H-reflex

0
Arms cycling
Soleus

-2 M-wave

-4
-0.1 0 0.02 0.04 0.06
Time
Time (sec)
(sec)

Zhou et al, 2018

30

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44th SCI/D Symposium 2021‐04‐08

Rhythmic arm cycling suppresses soleus H-

reflex in neurologically-intact individuals
(N = 10)
55%
*
SOL H-reflex peak-to-peak

SOL rest, arm at 0

(normalized to Mmax)

50%
SOL 10%MVC, arm at 0
SOL rest, arm at 90
45%
SOL 10%MVC, arm at 90
SOL rest, arm at 180
40%
SOL 10%MVC, arm at 180
SOL rest, arm at 270
35%
SOL 10%MVC, arm at 270

30%
arm STATIC arm CYCLING
Zhou et al, 2018

31

Effect of cycling training on cervico-lumbar

propriospinal regulation in iSCI

Soleus H-reflex Soleus H-reflex

(pre-training) (post-training)
SOL H-reflex amplitude (mv)

8 8

6 6 *
4 4

2 2

0 0
arms STATIC arms CYCLING arms STATIC arms CYCLING

Zhou et al, 2018

32

Summary of Findings

• Cycling translates to improvements in walking

• Active engagement of the arms (cervico-
lumbar networks) leads to larger improvements
in walking
• Underlying mechanisms include improvements
in corticospinal drive and cervico-lumbar
modulation
• Participants highly receptive of the intervention
and wanted to continue

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Ongoing Work

• Understanding the mechanisms of action of

transcutaneous spinal cord stimulation (tSCS) for
facilitating activation of spinal networks

34

Transcutaneous SC stimulation (tSCS)

Cathodes
C3
C6

T11
L1

Anodes

Barss et al, J Neurophysiol, 2019

Parhizi et al, Frontiers Neurosci (In Press)
35

Ongoing Work

• Understanding the mechanisms of action of

transcutaneous spinal cord stimulation (tSCS) for
facilitating activation of spinal networks

• Addition of tSCS to the cervical / lumbar cord during

cycling

• Investigating the effect of arm cycling alone with tSCS

• Effect of A&L cycling with cervical transcutaneous

stimulation in people with more severe SCIs (e.g., AIS
B)

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44th SCI/D Symposium 2021‐04‐08

Acknowledgements: People

Trevor Barss Behdad Parhizi

PhD PhD candidate

Rui Zhou Laura Alvarado, MSc

PhD Su Ling Chong, PT
Robert Ogilvie, MD
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Oriana Shaw, BSc

Acknowledgements:

Sensory
Motor
Adaptive
Rehabilitation
Technology

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