A brief background on motor unit physiology and some of the findings from my PhD research projects involving quantification of the neural command to the calf muscles and adjustments in neural drive in response to stretching.
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PhD Dissertation Defense - Melissa Mazzo - Estimates of neural drive and the control of muscle force.
1. Estimates of neural drive and
the control of muscle force
Dissertation Defense
Melissa Rose Mazzo
7/19/2021
2. Dissertation outline
Hamilton, L.D., Mazzo, M.R., Petrigna, L., Ahmed, A.A., & Enoka, R.M. Poor estimates of motor variability are
associated with longer grooved pegboard times for middle-aged and older adults. J Neurophysiol 121(2):
588–601, 2019.
Capobianco, R.A., Mazzo, M.R., & Enoka, R.M. Self-massage prior to stretching improves flexibility in young
and middle-aged adults. J Sports Sci 37(13): 1543–1550, 2019.
Mazzo M.R., Capobianco R.A., Holobar A., Enoka R.M. Changes in calf muscle strength after static stretching
are associated with adjustments in neural drive. Pilot data, unpublished, 2020.
Mazzo M.R., Weinman L.E., Giustino V., Mclagan B., Maldonado J., Enoka R.M. Changes in neural drive to calf
muscles during steady submaximal contractions after repeated static stretches. J Physiol – Accepted, 2021.
Mazzo M.R., Holobar, A., Enoka, R.M. Association between effective neural drive to the triceps surae muscles
and plantar-flexion torque during submaximal isometric contractions. In preparation, 2021.
3. Dissertation outline
1. Basics of motor unit physiology
2. Poor estimates of motor variability are associated with longer
grooved pegboard times for middle-aged and older adults
3. Self-massage with therapy balls improves flexibility in young and
middle-aged adults
4. Changes in calf muscle strength after static stretching are
associated with adjustments in neural drive
5. Changes in neural drive to calf muscles during steady submaximal
contractions after repeated static stretches
6. Association between effective neural drive to the triceps surae
muscles and plantar-flexion torque during submaximal isometric
contractions
4. Dissertation outline
1. Basics of motor unit physiology
2. Poor estimates of motor variability are associated with longer
grooved pegboard times for middle-aged and older adults
3. Self-massage with therapy balls improves flexibility in young and
middle-aged adults
4. Changes in calf muscle strength after static stretching are
associated with adjustments in neural drive
5. Changes in neural drive to calf muscles during steady submaximal
contractions after repeated static stretches
6. Association between effective neural drive to the triceps surae
muscles and plantar-flexion torque during submaximal isometric
contractions
5. Dissertation outline
1. Basics of motor unit physiology
2. Poor estimates of motor variability are associated with longer
grooved pegboard times for middle-aged and older adults
3. Self-massage with therapy balls improves flexibility in young and
middle-aged adults
4. Changes in calf muscle strength after static stretching are
associated with adjustments in neural drive
5. Changes in neural drive to calf muscles during steady submaximal
contractions after repeated static stretches
6. Association between effective neural drive to the triceps surae
muscles and plantar-flexion torque during submaximal isometric
contractions
Temporary adjustments in
motor unit activity in response
to stretch
Estimating neural drive to synergists
16. Motor neuron
Muscle
Muscle fibers
Spinal cord
5 spikes
per second
10 spikes
per second
20 spikes
per second
From spikes of activity to contractile force
Motor unit force
17. Importantly, it is the combination of activity of
all active motor units that produces muscle force
Neural drive to muscle
Neuron 1
Neuron 2
Neuron 3
Neuron 4
Neuron 5
18. Lateral force
transmission
Fascial & connective
tissue mechanics
Tendon properties
Spring-like
filament, Titin
Inter-muscular
connections
Aponeurosis
morphology
Generation & transmission of force
Contractile proteins
20. Dissertation outline
1. Basics of motor unit physiology
2. Poor estimates of motor variability are associated with longer
grooved pegboard times for middle-aged and older adults
3. Self-massage with therapy balls improves flexibility in young and
middle-aged adults
4. Changes in calf muscle strength after static stretching are
associated with adjustments in neural drive
5. Changes in neural drive to calf muscles during steady submaximal
contractions after repeated static stretches
6. Association between effective neural drive to the triceps surae
muscles and plantar-flexion torque during submaximal isometric
contractions
Temporary adjustments in
motor unit activity in response
to stretch
21. 3. Self-massage with therapy balls improves flexibility in young
and middle-aged adults
4. Changes in calf muscle strength after static stretching are
associated with adjustments in neural drive
Temporary adjustments in motor unit activity
Robyn Capobianco
22. 3. Self-massage with therapy balls improves flexibility in young
and middle-aged adults
4. Changes in calf muscle strength after static stretching are
associated with adjustments in neural drive
Primary aim:
To compare the influence of two flexibility-increasing
interventions on maximal torque capacity and motor unit
activity during submaximal muscle contractions.
Temporary adjustments in motor unit activity
23. Static stretching of the calf muscles:
Maximal range
of motion
Maximal voluntary
contraction torque
26. Str
pro
Con
pro
MVCs ROM
10% MVC
35% MVC
9 ± 2 min. 4 m
6 ± 1 min.
Testing before
A. Force apparatus
B.
Right leg
Force
transducer
Timing of experiment
Experimental setup: Isometric plantar flexion contractions
Plantar flexion
29. Maximal voluntary contraction torque: Variable responses
20
40
60
80
100
120
140
160
180
200
Stretch + SM
Before After Before After
Stretch
20
40
60
80
100
120
140
160
180
200
MVC
torque
(N
m)
Stretch + Massage Stretch
*
Maximal
calf strength
30. 5 min. after intervention
Medial
gastrocnemius
Soleus
High-density
electromyography
Right Leg
31. Identifying individual spikes of motor unit activity
Neuron / Motor unit 1
Neuron / Motor unit 2
Neuron / Motor unit 3
Neuron / Motor unit 4
Neuron / Motor unit 5
33. Submaximal contractions:
Because maximal strength changed, the amount of torque produced
during the 20%-of-maximum tasks changed
20% MVC Before
20% MVC After
MVC Before
MVC After
35. Submaximal contractions:
Because maximal strength changed, the amount of torque produced
during the 20%-of-maximum tasks changed
20% MVC Before
20% MVC After
MVC Before
MVC After
We normalized
motor unit activity
to the torque produced
36. Submaximal contractions: Individuals who had a decrease
in maximal torque capacity also had an increase in relative motor unit activity
20
40
60
80
100
120
140
160
180
200
Stretch + SM
Before After Before After
Stretch
20
40
60
80
100
120
140
160
180
200
MVC
torque
(N
m)
Stretch + Massage Stretch
37. Submaximal contractions: Motor unit discharge rate increased
despite a decrease in the torque being produced
16
18
20
24
22
Torque
(N•m)
stretch
stretch
5
0
10
15
20
25
Soleus
stretch
10 s
D.
After
Before
14.69 pps
13.68 pps
21.7 N•m
8.6 N•m
8.6 N•m
Medial gastrocnemius
9
10
11
12
13
14
15
Mean
discharge
rate
(pps)
20% MVC Before
20% MVC After
38. Lateral force
transmission
Fascial & connective
tissue mechanics
Tendon properties
Spring-like Titin
Activation
signal
required
Motor unit activity
relative to torque
produced
39. Lateral force
transmission
Fascial & connective
tissue mechanics
Tendon properties
Spring-like Titin
Force generation
and/or
transmission
Motor unit
activity
40. Temporary adjustments in motor unit activity
Similar adjustments in motor unit activity were observed
in response to both interventions
when maximal strength decreased.
41. 5. Changes in neural drive to calf muscles during steady
submaximal contractions after repeated static stretches
Primary aim:
To investigate the acute effects of static stretching
on motor unit activity of the plantar flexor muscles.*
Secondary aim:
To determine whether maximal muscle contractions
attenuate the effects of static stretching.
*Submaximal
contractions
performed at
the same
absolute
torque levels
Temporary adjustments in motor unit activity
42. Stretch
protocol
Control
protocol
MVCs ROM
10% MVC
35% MVC
9 ± 2 min. 4 min.
6 ± 1 min.
Testing before
A. Force apparatus
B.
Right leg
Force
transducer
Timing of experimental prot
Medial
Gastrocnemius
Lateral
Gastroc.
Soleus
Experimental setup:
Isometric plantar flexion contractions
High-density
electromyography
Right Leg
49. MG
LG
SOL
0
10% MVC
10% MVC
Plantar flexion force Soleus
Medial gastrocnemius
Lateral gastrocnemius
MG
0 40
10 50
30
20 60
Composite plantar-flexor spike train: Combined activity of MG, LG and SOL
A. B. C.
D.
Time (s)
0
10% MVC
10% MVC
Plantar flexion force Soleus
Medial gastrocnemius
Lateral gastrocnemius
MG
0 40
10 50
30
20 60
Composite plantar-flexor spike train: Combined activity of MG, LG and SOL
A. B. C.
D.
51. 0 1
10% MVC
10% MVC
Plantar flexion force Soleus
Medial gastrocnemius
Lateral gastrocnemius
MG
0 40
10 50
30
20 60
Composite plantar-flexor spike train: Combined activity of MG, LG and SOL
A. B. C.
D.
Time (s)
Cumulative plantar-flexor spike train
MG LG
SOL
52. Time (s)
Cumulative plantar flexor spike train
Cumulative
plantar
flexor
spike
train
(AU)
Smoothed motor unit activity of
ALL calf muscles:
(total neural drive to the calf muscles)
MG LG
SOL
53. All motor units identified Matched motor units
Intervention
protocol
Submaximal
contraction Before After
After
MVCs Total
Unique
units
Mean ± SD
per trial
Before vs.
After
After vs.
After
MVCs
Across all
time
points
Stretch
10% MVC 347 447 392 1186 550 24.1 ± 15 276 334 212
35% MVC 364 390 395 1149 354 22.2 ± 12 263 349 265
Control
10% MVC 395 414 406 1215 441 23.4 ± 15 276 357 258
35% MVC 385 384 398 1167 270 21.6 ± 12 313 367 299
A total of 1,615 unique motor units were identified:
58. Results: Cumulative plantar-flexor spike train*
Cumulative plantar flexor spike train
Cumulative
plantar
flexor
spike
train
(AU)
*Value depends on
the number
of identified
motor units
61. Results: Recruitment thresholds
10% MVC
3.6% MVC
5.2% MVC
9.8% MVC
Plantar
flexor
torque
The force at which motor units
are recruited or “activated”
63. Results: At 10% MVC after static stretching
Mean discharge rate (averaged by muscle)
Estimate of total neural drive to the plantar flexors
Earlier recruitment of motor units
These changes were partially
resolved after the maximal
calf-muscle contractions.
64. Results: 35% MVC
No influence of repeated static stretching on motor unit discharge rate,
recruitment threshold or estimated neural drive to the plantar flexors.
65. Conclusions:
Stretching increases the amount of motor unit activity required to produce a
given submaximal force.
However, this was only observed at low force levels (10% MVC).
67. Lateral force
transmission
Fascial & connective
tissue mechanics
Tendon properties
Spring-like
filament, Titin
Inter-muscular
connections
Aponeurosis
morphology
This indicates that stretching altered the properties of
the muscle and/or connective tissue:
• Increased compliance
of the muscle-tendon unit
• Less efficient force
generation/transmission
68.
69.
70. Estimating neural drive from motor unit activity
Neural drive to muscle
Neuron 1
Neuron 2
Neuron 3
Neuron 4
Neuron 5
Total amount of electrical
activity in the muscle
71. For single-muscle
actions, cumulative
motor unit activity is
highly correlated
with force output
EMG
R = 0.49
CST
R = 0.81
Soleus
Force
Smoothed EMG amplitude
Cumulative spike train (CST)
Adapted form Thompson et al., 2018
72. Primary component of fluctuations in discharge rates
Smoothed EMG amplitude
For single-muscle
actions, cumulative
motor unit activity is
highly correlated
with force output
Abductor digiti minimi
Torque
R = 0.35
R = 0.65
Adapted form Negroet al., 2009
73. Cumulative spike train
neural drive to muscle
Primary component of
fluctuations
in discharge rates
Estimates of neural drive to
muscle using cumulative
motor unit activity
74. Neural control of the calf muscles
Primary aim:
To determine whether estimates of neural drive created from the motor
unit activity of three synergist calf muscles accurately predict net plantar
flexion torque.
Secondary aim:
To determine whether motor unit number influences the
accuracy of the estimates of neural drive.
6. Association between effective neural drive to the triceps surae
muscles and plantar-flexion torque during submaximal
isometric contractions
85. 10% MVC 35% MVC
CST FPC CST FPC
Similarity between estimates of neural drive and torque: Entire 30 s
*
86. 10% MVC 35% MVC
CST FPC CST FPC
Similarity between estimates of neural drive and torque: Shorter windows
*
*
87. 10% MVC 35% MVC
CST FPC CST FPC
Similarity between estimates of neural drive and torque: Shorter windows
*
*
88. CST or FPC as an estimate of neural drive:
On average, both estimates were moderately correlated with plantar flexion
torque.
If the goal is to accurately predict plantar flexion torque during steady force
production, the cross correlation between CST estimates and torque were:
• More consistent than the FPC
• Slightly stronger than the FPC when analyzing the entire steady portion
• Correlation with torque was less inflated by short window lengths
90. Influence of motor unit number: CST estimate or neural drive
Significant influence of
motor unit number on the
cross correlation between
the CST and torque at
35% MVC.
5
39
However, there is large
variability!
91. Even though the CST may be our top choice for estimating the
total neural drive to synergist muscles…
FPC
92. 68% of the variance in discharge rates
is explained by the FPC
28% of the variance in discharge rates
is explained by the FPC
Ability of the FPC to explain fluctuations in discharge rate:
*
*
*
93. Ability of the FPC to explain fluctuations in discharge rate:
Influence of motor unit number
94. Ability of the FPC to explain fluctuations in discharge rate:
Influence of motor unit number
35% MVC
5-s windows
95. When the first principal component could describe a greater proportion
of the fluctuations in motor unit discharge rates…
…neural drive and torque were more correlated.
Mean of 5-s windows
96. When the motor units from all three calf muscles were increasing
or decreasing their activity in unison…
…the estimates of neural drive better
predicted net plantar-flexion torque.
97. Conclusions: Estimating neural drive to synergist muscles
Cumulative motor unit activity from a group of synergist muscles can
reasonably predict net joint torque in most individuals.
A principal component analysis is not necessary to generate a reasonable
estimate of neural drive — a smoothed sum of motor unit activity is less
variable and usually more strongly correlated with torque during steady force
production.
The ability of estimated neural drive to predict net torque is somewhat
dependent on the number of motor units identified in the EMG.
98. Conclusions: Translation to tasks of daily life
The ability to produce steady force with the calf muscles is associated with:
• Postural sway during standing balance
• Performance on tests of walking speed
Plantar-flexion force steadiness is also likely to contribute to:
• Steady driving ability (fewer fluctuations with the gas pedal)
• How long you can hold the chair pose on your toes in yoga
• Walking across a log over a cold mountain creek
• Balance while wearing high heels
99. Robust static stretching may alter musculotendinous properties.
The nervous system adjusts the neural command to muscle when
force generation and transmission capabilities are altered.
The neural command underlying a single joint action produced
by synergist muscles is variable across individuals, but can be
predicted fairly well by the sum of motor unit activity.
Final conclusions: