Articles in PresS. J Appl Physiol (March 12, 2015). doi:10.1152/japplphysiol.00553.2014
1
Title: Torque decrease during submaximal evoked contractions of the quadriceps muscle is
2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
not only linked to muscle fatigue
19
20
Laboratoire INSERM U1093
21
Université de Bourgogne
22
Faculté des Sciences du Sport
23
Campus Universitaire Montmuzard
24
BP 27877
25
21078 Dijon Cedex
26
FRANCE
Boris Matkowski, Romuald Lepers and Alain Martin.
Laboratoire INSERM U1093, Cognition, Action et Plasticité Sensorimotrice, Université de Bourgogne, Faculté des Sciences du Sport, Dijon, France.
Running title: Muscle fatigue during evoked contraction
Corresponding author: Boris Matkowski
27 28
E-mail: [email protected]
29
Tel.: +33 (0)3-80-39-67-61
30
Fax: +33 (0)3-80-39-67-49
31
1 Copyright © 2015 by the American Physiological Society.
32
Abstract
33
The aim of this study was to analyze the neuromuscular mechanisms involved in the torque
34
decrease induced by submaximal electromyostimulation (EMS) of the quadriceps muscle. It
35
was hypothesized that torque decrease after EMS would reflect the fatigability of the activated
36
motor units (MUs), but also a reduction in the number of MUs recruited due to changes in
37
axonal excitability threshold. Two experiments were performed on twenty male subjects in
38
order to analyze i) the supramaximal twitch superimposed and evoked at rest during EMS
39
(experiment 1, n = 9), and ii) the twitch response and torque-frequency relation of the MUs
40
activated by EMS (experiment 2, n = 11). Torque loss was assessed by 15 EMS-evoked
41
contractions (50 Hz, 6-s on/6-s off), elicited at a constant intensity that evoked 20% of the
42
maximal voluntary contraction (MVC) torque. The same stimulation intensity delivered over
43
the muscles was used to induce the torque-frequency relation and the single electrical pulse
44
evoked after each EMS contraction (experiment 2). In experiment 1, supramaximal twitch
45
was induced by femoral nerve stimulation. Torque decreased by ∼60% during EMS-evoked
46
contractions and by only of ∼18% during MVCs. This was accompanied by a rightward shift
47
of the torque-frequency relation of MUs activated and an increase of the ratio between the
48
superimposed and post-tetanic maximal twitch evoked during EMS contraction. These
49
findings suggest that the torque decrease observed during submaximal EMS-evoked
50
contractions involved muscular mechanisms but also a reduction in the number of MUs
51
recruited due to changes in axonal excitability.
52 53
Keywords: electrical stimulation, femoral nerve stimulation, isometric contraction, torque-
54
frequency relation.
2
55
Introduction
56
Electromyostimulation (EMS) is a technique, applied over the muscle or the nerve,
57
that evokes muscle contraction via activation of both, motor and sensory axons (10, 15, 19),
58
generating in that way contractions through peripheral and central pathways (5, 13, 19). This
59
pattern of motor units (MUs) activation differs from voluntary contractions (17, 38), leading
60
to exaggerated metabolic demand and greater force loss compared to voluntary exercise
61
performed at the same intensity (21, 28, 37, 40).
62
The greater fatigability and discomfort associated with EMS have limited its clinical
63
use. To improve its application, numerous researchers have focused on determining the
64
stimulation protocol that minimize fatigability and increases muscle performance (7, 8, 39).
65
Most studies have been performed on able-bodied subjects quantifying fatigability as the
66
percent decline of the electrically evoked torque between the beginning and the end of the
67
fatiguing exercise (start-end torque index) (7, 8, 17, 39). However, this torque decrease does
68
not reflect the functional impact of the stimulation protocol on the force-generating capacity
69
of an individual, as assessed by the maximal voluntary contraction (MVC). Indeed, greater
70
declines in torque have been observed after EMS exercises evoked at constant and variable
71
stimulation frequencies compared with MVC torque (30, 31). Moreover, similar results were
72
observed when the maximal twitch was compared with one elicited at the stimulation
73
intensity used during the EMS exercise (31). These contrasting results relating to torque
74
losses between MVC and evoked contractions suggest that mechanisms, other than the
75
fatigability of the activated MUs, contribute to the decline in torque during an EMS protocol.
76
The potential mechanisms that may contribute to the greater torque decline during
77
submaximal fatiguing EMS include an increase in the excitability threshold of the active
78
axons due to repetitive stimulation leading to a decrease in the number of active axons and
79
thus contributing to torque decrease (4, 12, 23).
3
80
To investigate the possible reduction in the number of MUs recruited during EMS
81
fatiguing exercise, related to change in excitability threshold of active axons, the twitch
82
interpolation technique can be used. This technique, initially developed by Merton (29) for
83
the adductor pollicis muscle, and subsequently widely used for other muscle groups such as
84
the quadriceps femoris muscle (3, 27, 33), relies on the comparison of the maximal twitch
85
force produced by a supramaximal nerve stimulation evoked at rest to that produced by the
86
same stimulus superimposed on a voluntary contraction. The extra force developed by the
87
interpolated twitch provides a quantification of the proportion of the muscle force that is not
88
involved in the voluntary effort. This technique, previously used during a tetanic contraction
89
of human adductor pollicis (16), can be applied during submaximal EMS fatiguing
90
contractions to quantify the proportion of the MUs not activated by the electrical stimulation,
91
thus providing information on a reduction in the number of MUs recruited during repetitive
92
electrical stimulation.
93
The aim of the present study was to evaluate the possible mechanisms involved in
94
EMS-evoked fatigue by measuring i) the maximal twitch evoked at rest and superimposed
95
during EMS, and ii) the mechanical response and torque-frequency relation of the activated
96
muscle. We hypothesized that the torque decrease at the end of EMS protocol would reflect
97
not only the fatigability of the activated MUs, but also a reduction in the number of MUs
98
recruited due to changes in axonal excitability threshold.
99
4
100
Materials and methods
101
Subjects
102
20 healthy men (Experiment 1: n = 9, age: 27.4 ± 6.9 years, height: 176.0 ± 5.1 cm,
103
mass: 70.7 ± 7.1 kg; mean ± SD; Experiment 2: n = 11, age: 26.4 ± 5.7 years, height: 179.1 ±
104
5.8 cm, mass: 76.3 ± 7.0 kg) volunteered to participate in the present study and were tested
105
before, during and after fatiguing contractions elicited by EMS. None of them had any known
106
neurological or neuromuscular disorder. Each individual was informed about the experimental
107
procedures and possible risks and provided informed consent prior participating in the study.
108
The University of Burgundy committee on Human Research approved the protocol. The study
109
was conducted according to the Declaration of Helsinki.
110 111
Torque measurements
112
Mechanical measurements were performed using an isokinetic dynamometer (Biodex,
113
Shirley Corporation, New York, USA) in an isometric mode. The axis of the dynamometer
114
was aligned with the flexion-extension axis of rotation for the knee, and a strap attached the
115
lever arm to the shank. The upper body was restrained with two crossover shoulder harnesses
116
and a belt across the abdomen. Experiments were performed on the right (dominant) leg with
117
knee and hip joint angles of 90°. Subjects were asked to cross their arms over the chest during
118
the testing procedure.
119 120
Electromyostimulation (EMS)
121
EMS of the quadriceps muscle was applied with a high voltage (maximal voltage 400
122
V) constant-current stimulator (model DS7A, Digitimer, Hertfordshire, United Kingdom) to
123
evoke repeated tetanic contractions. Two large electrodes were placed on the anterior aspect
124
of the thigh. The cathode (10 × 5 cm, Compex SA, Ecublens, Switzerland) was placed distally
5
125
at 10 cm above the upper border of the patella over vastus lateralis (VL), vastus medialis
126
(VM) and rectus femoris (RF) muscles. The anode (10 × 5 cm) was placed at ~5 cm below the
127
inguinal ligament. A pulse duration of 1-ms was used and the current was set so that 50 Hz
128
stimulation elicited 20% of the MVC torque developed before the fatiguing exercise (see
129
below). The required current (range: 26-68 mA) caused only mild discomfort and no
130
noticeable voluntary contractions during EMS-evoked contractions. For the second
131
experiment, this intensity was also used to induce a single twitch after each EMS-evoked
132
contraction and the torque-frequency relation recorded before and after the fatiguing exercise.
133 134
Femoral nerve stimulation
135
The femoral nerve was stimulated with a second constant-current stimulator (model
136
DS7A, Digitimer) to evoke maximal single twitches during (superimposed twitch) and after
137
EMS-evoked contractions. The femoral nerve was stimulated with a 1-ms pulse using a
138
cathode ball electrode (0.5 cm diameter) pressed into the femoral triangle by the same
139
experimenter during all testing sessions. The anode was a 10 × 5 cm rectangular electrode
140
(Compex SA, Ecublens, Switzerland) located in the gluteal fold opposite the cathode. The
141
stimulus current was considered maximal when an increase in the current no longer increased
142
the amplitude of the twitch torque or the peak-to-peak amplitude of the compound muscle
143
action potentials (M wave; see below). The current intensity was increased by 25%, and this
144
supramaximal stimulus intensity was used throughout the experiment (range: 60-90 mA).
145 146
Electromyography
147
The electromyographic (EMG) signals were recorded in VL, VM, and RF using pairs
148
of silver-silver chloride (10 mm diameter; 20 mm between electrodes) electrodes (Controle
149
Graphique Medical, Brie-Comte-Robert, France) positioned over each muscle according to
6
150
the SENIAM recommendations. The recording sites were adjusted in pilot testing to detect
151
the greatest M-wave amplitude at a given intensity for each knee extensor muscle (33). The
152
reference electrode was attached to the patella of the left knee. The skin was abraded and
153
cleaned with alcohol to minimize the resistance between the two electrodes (
1
Title: Torque decrease during submaximal evoked contractions of the quadriceps muscle is
2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
not only linked to muscle fatigue
19
20
Laboratoire INSERM U1093
21
Université de Bourgogne
22
Faculté des Sciences du Sport
23
Campus Universitaire Montmuzard
24
BP 27877
25
21078 Dijon Cedex
26
FRANCE
Boris Matkowski, Romuald Lepers and Alain Martin.
Laboratoire INSERM U1093, Cognition, Action et Plasticité Sensorimotrice, Université de Bourgogne, Faculté des Sciences du Sport, Dijon, France.
Running title: Muscle fatigue during evoked contraction
Corresponding author: Boris Matkowski
27 28
E-mail: [email protected]
29
Tel.: +33 (0)3-80-39-67-61
30
Fax: +33 (0)3-80-39-67-49
31
1 Copyright © 2015 by the American Physiological Society.
32
Abstract
33
The aim of this study was to analyze the neuromuscular mechanisms involved in the torque
34
decrease induced by submaximal electromyostimulation (EMS) of the quadriceps muscle. It
35
was hypothesized that torque decrease after EMS would reflect the fatigability of the activated
36
motor units (MUs), but also a reduction in the number of MUs recruited due to changes in
37
axonal excitability threshold. Two experiments were performed on twenty male subjects in
38
order to analyze i) the supramaximal twitch superimposed and evoked at rest during EMS
39
(experiment 1, n = 9), and ii) the twitch response and torque-frequency relation of the MUs
40
activated by EMS (experiment 2, n = 11). Torque loss was assessed by 15 EMS-evoked
41
contractions (50 Hz, 6-s on/6-s off), elicited at a constant intensity that evoked 20% of the
42
maximal voluntary contraction (MVC) torque. The same stimulation intensity delivered over
43
the muscles was used to induce the torque-frequency relation and the single electrical pulse
44
evoked after each EMS contraction (experiment 2). In experiment 1, supramaximal twitch
45
was induced by femoral nerve stimulation. Torque decreased by ∼60% during EMS-evoked
46
contractions and by only of ∼18% during MVCs. This was accompanied by a rightward shift
47
of the torque-frequency relation of MUs activated and an increase of the ratio between the
48
superimposed and post-tetanic maximal twitch evoked during EMS contraction. These
49
findings suggest that the torque decrease observed during submaximal EMS-evoked
50
contractions involved muscular mechanisms but also a reduction in the number of MUs
51
recruited due to changes in axonal excitability.
52 53
Keywords: electrical stimulation, femoral nerve stimulation, isometric contraction, torque-
54
frequency relation.
2
55
Introduction
56
Electromyostimulation (EMS) is a technique, applied over the muscle or the nerve,
57
that evokes muscle contraction via activation of both, motor and sensory axons (10, 15, 19),
58
generating in that way contractions through peripheral and central pathways (5, 13, 19). This
59
pattern of motor units (MUs) activation differs from voluntary contractions (17, 38), leading
60
to exaggerated metabolic demand and greater force loss compared to voluntary exercise
61
performed at the same intensity (21, 28, 37, 40).
62
The greater fatigability and discomfort associated with EMS have limited its clinical
63
use. To improve its application, numerous researchers have focused on determining the
64
stimulation protocol that minimize fatigability and increases muscle performance (7, 8, 39).
65
Most studies have been performed on able-bodied subjects quantifying fatigability as the
66
percent decline of the electrically evoked torque between the beginning and the end of the
67
fatiguing exercise (start-end torque index) (7, 8, 17, 39). However, this torque decrease does
68
not reflect the functional impact of the stimulation protocol on the force-generating capacity
69
of an individual, as assessed by the maximal voluntary contraction (MVC). Indeed, greater
70
declines in torque have been observed after EMS exercises evoked at constant and variable
71
stimulation frequencies compared with MVC torque (30, 31). Moreover, similar results were
72
observed when the maximal twitch was compared with one elicited at the stimulation
73
intensity used during the EMS exercise (31). These contrasting results relating to torque
74
losses between MVC and evoked contractions suggest that mechanisms, other than the
75
fatigability of the activated MUs, contribute to the decline in torque during an EMS protocol.
76
The potential mechanisms that may contribute to the greater torque decline during
77
submaximal fatiguing EMS include an increase in the excitability threshold of the active
78
axons due to repetitive stimulation leading to a decrease in the number of active axons and
79
thus contributing to torque decrease (4, 12, 23).
3
80
To investigate the possible reduction in the number of MUs recruited during EMS
81
fatiguing exercise, related to change in excitability threshold of active axons, the twitch
82
interpolation technique can be used. This technique, initially developed by Merton (29) for
83
the adductor pollicis muscle, and subsequently widely used for other muscle groups such as
84
the quadriceps femoris muscle (3, 27, 33), relies on the comparison of the maximal twitch
85
force produced by a supramaximal nerve stimulation evoked at rest to that produced by the
86
same stimulus superimposed on a voluntary contraction. The extra force developed by the
87
interpolated twitch provides a quantification of the proportion of the muscle force that is not
88
involved in the voluntary effort. This technique, previously used during a tetanic contraction
89
of human adductor pollicis (16), can be applied during submaximal EMS fatiguing
90
contractions to quantify the proportion of the MUs not activated by the electrical stimulation,
91
thus providing information on a reduction in the number of MUs recruited during repetitive
92
electrical stimulation.
93
The aim of the present study was to evaluate the possible mechanisms involved in
94
EMS-evoked fatigue by measuring i) the maximal twitch evoked at rest and superimposed
95
during EMS, and ii) the mechanical response and torque-frequency relation of the activated
96
muscle. We hypothesized that the torque decrease at the end of EMS protocol would reflect
97
not only the fatigability of the activated MUs, but also a reduction in the number of MUs
98
recruited due to changes in axonal excitability threshold.
99
4
100
Materials and methods
101
Subjects
102
20 healthy men (Experiment 1: n = 9, age: 27.4 ± 6.9 years, height: 176.0 ± 5.1 cm,
103
mass: 70.7 ± 7.1 kg; mean ± SD; Experiment 2: n = 11, age: 26.4 ± 5.7 years, height: 179.1 ±
104
5.8 cm, mass: 76.3 ± 7.0 kg) volunteered to participate in the present study and were tested
105
before, during and after fatiguing contractions elicited by EMS. None of them had any known
106
neurological or neuromuscular disorder. Each individual was informed about the experimental
107
procedures and possible risks and provided informed consent prior participating in the study.
108
The University of Burgundy committee on Human Research approved the protocol. The study
109
was conducted according to the Declaration of Helsinki.
110 111
Torque measurements
112
Mechanical measurements were performed using an isokinetic dynamometer (Biodex,
113
Shirley Corporation, New York, USA) in an isometric mode. The axis of the dynamometer
114
was aligned with the flexion-extension axis of rotation for the knee, and a strap attached the
115
lever arm to the shank. The upper body was restrained with two crossover shoulder harnesses
116
and a belt across the abdomen. Experiments were performed on the right (dominant) leg with
117
knee and hip joint angles of 90°. Subjects were asked to cross their arms over the chest during
118
the testing procedure.
119 120
Electromyostimulation (EMS)
121
EMS of the quadriceps muscle was applied with a high voltage (maximal voltage 400
122
V) constant-current stimulator (model DS7A, Digitimer, Hertfordshire, United Kingdom) to
123
evoke repeated tetanic contractions. Two large electrodes were placed on the anterior aspect
124
of the thigh. The cathode (10 × 5 cm, Compex SA, Ecublens, Switzerland) was placed distally
5
125
at 10 cm above the upper border of the patella over vastus lateralis (VL), vastus medialis
126
(VM) and rectus femoris (RF) muscles. The anode (10 × 5 cm) was placed at ~5 cm below the
127
inguinal ligament. A pulse duration of 1-ms was used and the current was set so that 50 Hz
128
stimulation elicited 20% of the MVC torque developed before the fatiguing exercise (see
129
below). The required current (range: 26-68 mA) caused only mild discomfort and no
130
noticeable voluntary contractions during EMS-evoked contractions. For the second
131
experiment, this intensity was also used to induce a single twitch after each EMS-evoked
132
contraction and the torque-frequency relation recorded before and after the fatiguing exercise.
133 134
Femoral nerve stimulation
135
The femoral nerve was stimulated with a second constant-current stimulator (model
136
DS7A, Digitimer) to evoke maximal single twitches during (superimposed twitch) and after
137
EMS-evoked contractions. The femoral nerve was stimulated with a 1-ms pulse using a
138
cathode ball electrode (0.5 cm diameter) pressed into the femoral triangle by the same
139
experimenter during all testing sessions. The anode was a 10 × 5 cm rectangular electrode
140
(Compex SA, Ecublens, Switzerland) located in the gluteal fold opposite the cathode. The
141
stimulus current was considered maximal when an increase in the current no longer increased
142
the amplitude of the twitch torque or the peak-to-peak amplitude of the compound muscle
143
action potentials (M wave; see below). The current intensity was increased by 25%, and this
144
supramaximal stimulus intensity was used throughout the experiment (range: 60-90 mA).
145 146
Electromyography
147
The electromyographic (EMG) signals were recorded in VL, VM, and RF using pairs
148
of silver-silver chloride (10 mm diameter; 20 mm between electrodes) electrodes (Controle
149
Graphique Medical, Brie-Comte-Robert, France) positioned over each muscle according to
6
150
the SENIAM recommendations. The recording sites were adjusted in pilot testing to detect
151
the greatest M-wave amplitude at a given intensity for each knee extensor muscle (33). The
152
reference electrode was attached to the patella of the left knee. The skin was abraded and
153
cleaned with alcohol to minimize the resistance between the two electrodes (
