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Theses
2011
Effects of ageing and Tai Chi training on soleus H-reflex in older adultsYung-Sheng ChenSouthern Cross University
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Publication detailsChen, YS 2011, 'Effects of ageing and Tai Chi training on soleus H-reflex in older adults', PhD thesis, Southern Cross University,Lismore, NSW.Copyright YS Chen 2011
Effects of ageing and Tai Chi training on soleus H-reflex in older adults
Yung-Sheng Chen
Master of Science in Sport Sciences
This thesis is presented in fulfilment of the requirements for the degree of
Doctor of Philosophy at Southern Cross University
February 2011
ii
Declaration
I certify that the work presented in this thesis is, to the best of my knowledge and belief,
original, except as acknowledged in the text, and that the material has not been
submitted, either in whole or in part, for a degree at this or any other university.
I acknowledge that I have read and understood the Universitys rules, requirements,
procedures and policy relating to my higher degree research award and to my thesis, I
certify that I have complied with the rules, requirements, procedures and policy of the
University (as they may be from time to time).
Print Name: Yung-Sheng Chen
Signature:
Date: 02/02/2011
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Abstract
The Hoffmann reflex (H-reflex) is used to investigate the influence of Ia afferent
projection on the spinal motoneuron activities. It has been suggested that the H-reflex is
task-dependent and demonstrates adaptations to exercise training. Much of the previous
research on the H-reflex was based on young populations. Little information is available
on the H-reflex modulation in response to exercise and training in older populations.
The objective of the research work presented in this thesis was to expand our knowledge
on the effects of ageing and Tai Chi (TC) training on the soleus (SOL) H-reflex
modulations in older adults. Four related studies have been conducted.
Study I. The aim of this study was to determine the test-retest reliability of SOL H-
reflex assessment during isometric muscle contraction at various intensities and ankle
joint positions. The H-reflex was assessed when the ankle joint was placed at neutral
(0), plantarflexion 20, and dosiflexion 20 positions and during isometric
plantarflexion at 10%, 30% and 50% of the maximal voluntary contraction (MVC)
levels, on two separate days, in a group of young adults (5 males and 5 females, age
24.9 5 years). The results showed a high level of test-retested reliability (Intraclass
Correlation Coefficients, ICC) for the SOL H-reflex tested at the neutral (ICC = 0.96)
and plantarflexion (ICC = 0.92) positions, and a moderate level of ICC at the
dorsiflexion position (ICC = 0.75) during rest. The results also demonstrated that
assessing the SOL H-reflex during low intensity (10% MVC) of isometric muscle
contractions yielded more reliable test-retest outcomes (ICC = 0.92 0.95) than that
during contractions at higher intensities (30% and 50% MVC, ICC = 0.62 0.97),
regardless of ankle joint positions.
Study II. The aim of this study was to use a cross-sectional research design to compare
the effects of ankle joint position and muscle contraction intensity on SOL H-reflex gain,
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latency and duration between young (10 males and 10 females, age 25.1 4.0 years)
and older (10 males and 10 females, age 74.2 5.1 years) adults. The results showed
that there were significant differences of the SOL H-reflex parameters between young
and older adults under all testing conditions. However, when contraction intensity was
progressively increased, a similar down-regulation of the SOL H-reflex gain was
observed in both aged groups. This result may indicate a possible reservation of motor
function regulated by the supraspinal mechanisms in older adults.
Study III. The aim of this study was to investigate the effect of ageing on soleus (SOL)
H-reflex modulation during shortening and lengthening muscle actions. Cross-sectional
comparisons of the maximal amplitude of H-reflex (Hmax) and maximal amplitude of M-
wave (Mmax) ratio were made between young (10 males and 10 females, age 24.4 4.0
years) and older (10 males and 10 females, age 73.3 5.0 years) adults during passive
movements and voluntary contractions of the muscles around the ankle joint. The H-
reflex modulation during upright standing under eyes open/closed and on
stable/unstable surface conditions were also investigated in this study. The correlations
of SOL Hmax between these dynamic muscle actions and postural tasks were evaluated.
The results indicated that there were significant age-related differences of the SOL H-
reflex modulation during passive and active shortening and lengthening muscle actions.
Pearson correlation analysis revealed that the SOL Hmax during both the passive and
active shortening and lengthening plantarflexions was significantly correlated with that
during the postural tasks in young adults. However, older adults only demonstrated a
significant correlation of the SOL Hmax between the passive shortening and lengthening
actions and postural tasks.
Study IV. The aim of this study was to investigate the effects of 12 weeks of TC training
on the SOL H-reflex during upright standing under different visual and somatosensory
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conditions in older adults. Thirty-four volunteers (17 males and 17 females, age 72.9
5.9 years) were assigned into a TC and a control group. The results demonstrated that
the SOL Hmax/Mmax ratios during upright standing under eyes open/closed and
stable/unstable surface conditions were significantly increased after the TC training in
older adults. However, the mean displacements of centre of pressure (COP) in anterior-
posterior and medial-lateral directions were not significantly changed after training. The
results suggested that adaptive change of the SOL H-reflex is not related to control of
static posture after 12 weeks TC training in older adults.
This thesis demonstrated the age-related differences in the SOL H-reflex modulations
during different ankle joint positions, isometric and dynamic ankle muscle actions and
static upright standing. The adaptive change of the SOL H-reflex to 12 weeks of TC
training may provide insight into the understanding of the neural adaptation to TC
training in older adults.
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List of publications
Book chapter
Chen, Y. S., & Zhou, S. (2011). H-reflex assessment as a tool for understanding motor
functions in postural control. In Posture: Types, Assessment, and Control. New
York: Nova Science Publishers (in press).
Journal publications
Chen, Y. S., Zhou, S., Cartwright, C., Crowley, Z., Baglin, R. & Wang, F. (2010). Test-
retest reliability of the soleus H-reflex is affected by joint positions and muscle
force levels. Journal of Electromyography and Kinesiology, 20 (5), 980-987.
Chen, Y. S. & Zhou S. (2011). Soleus H-reflex and its relation to static postural control.
Gait and Posture, 33 (2), 169-178.
Chen, Y. S., Zhou, S., & Cartwright, C. (2011). Effect of 12 weeks Tai Chi training on
soleus H-reflex and control of static posture in older adults. Archives of
Physical Medicine and Rehabilitation, 92, 886-891.
Chen, Y. S., Crowley Z, Zhou S, Cartwright C. 2011 (submitted). Effect of 12 weeks
Tai Chi training on soleus H-reflex in older adults: a pilot study. European
Journal of Applied Physiology (submitted and under review).
vii
Conference publications
Chen, Y. S., Zhou, S., Cartwright, C., Crowley, Z., Baglin, R. & Wang, F. (2009). Test-
retest reliability of the soleus H-reflex is affected by joint positions and force
levels. Paper presented at the 8 th Annual Conference of the Society of Chinese
Scholars on Exercise Physiology and Fitness, Baptist University, Hong Kong,
China. Abstracts Book (pp 38).
Chen, Y. S., Zhou, S., Cartwright, C. & Crowley, Z. (2010). Effects of joint position
and muscle contraction intensity on soleus H-reflex in young and older adults.
Paper presented at the 4th The Australian Association for Exercise & Sports
Science Conference, Gold Coast, Australia. Abstracts Book (pp 79).
Chen, Y. S., Zhou, S. & Cartwright, C. (2010). Effect of ageing on soleus H-reflex
modulation during shortening and lengthening muscle actions. Paper presented
at the 9 th Annual Conference of the Society of Chinese Scholars on Exercise
Physiology and Fitness, Beijing Sport University, Beijing, China.
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Acknowledgments
I would like to express appreciation to my principal supervisor, Professor Shi Zhou and
co-supervisor, Professor Colleen Cartwright, for their guidance to my research and
amount of time they spent on providing feedback on the thesis, that are invaluable to my
study and academic development. Their practical advice, knowledge, and comments are
very much appreciated.
Thank Robert Baglin for his generous and skilful assistance with technical support and
computer setting for data acquisition.
Also, I would like to express my gratitude to Erich Wittstock. You are always available
when I need assistance and support in the laboratory.
Thank Zac Crowley for the initial encouragement of this study.
Also extensive thanks to Li Zhang from the Library, for her helpful consultation with
the Endnote program.
Furthermore, thank Fang Wang, for her assistance during testing and data collection.
A sincere gratitude to Dr. Pedro Bezerra for his practical advice on protocol design and
technical consultation for constructing my first study.
Thank also all participants and workmates who volunteered and cooperated for this
study. I am grateful to your commitments in time and efforts in participation of my
studies.
Finally, I want to express my sincere thanks to all the members of my family for their
full support and encouragement over the time of my Ph.D. candidature.
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Table of Contents
Declaration ......................................................................................................................ii
Abstract. .....................................................................................................................iii List of publications ........................................................................................................vi
Book chapter............................................................................................................vi
Journal publications.................................................................................................vi Conference publications .........................................................................................vii
Acknowledgments........................................................................................................viii
Table of Contents...........................................................................................................ix List of Figures ..............................................................................................................xiii
List of Tables.................................................................................................................xv Abbreviation ................................................................................................................xvi Units of measurement................................................................................................xviii Chapter 1 Introduction .............................................................................................1
1.1. Introduction ...........................................................................................................2 1.2. Aims of the investigation.......................................................................................9 1.3. Research hypotheses............................................................................................11
1.4. Significance of the research.................................................................................12 1.5. Study Limitations ................................................................................................12 1.6. Delimitation .........................................................................................................13 1.7. Ethical approval ...................................................................................................13
Chapter 2 Literature review...................................................................................14 2.1. Introduction .........................................................................................................15 2.2. Validity and reliability of H-reflex measurement................................................16
2.2.1. H-wave and M-wave ....................................................................................16 2.2.2. Reliability of H-reflex ..................................................................................19 2.2.3. Methodological concerns in H-reflex assessment ........................................20 2.2.4. Limitations of H-reflex test ..........................................................................27
2.3. Control of posture................................................................................................28
2.3.1. Sensory inputs ..............................................................................................28 2.3.2. Supraspinal mechanisms ..............................................................................30
2.3.3. Spinal mechanisms .......................................................................................33 2.4. H-reflex modulation in relation to control of static posture ................................41
2.4.1. Biomechanical characteristics of standing ...................................................41
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2.4.2. H-reflex modulation during postural tasks ...................................................42 2.4.3. Effect of balance training on H-reflex modulation.......................................46
2.5. Effect of Tai Chi training on neuromuscular adaptations in older adults............48 2.5.1. Muscular adaptations....................................................................................49 2.5.2. Neural adaptations ........................................................................................49
2.6. Summary..............................................................................................................50 Chapter 3 General methodology ............................................................................51
3.1. Recruitment of Participants .................................................................................52 3.2. H-reflex test .........................................................................................................55 3.3. Isometric submaximal voluntary contraction ......................................................57 3.4. Passive and active dynamic muscle actions ........................................................59 3.5. Static postural tasks .............................................................................................60 3.6. Data acquisition and analysis ..............................................................................61 3.7. Statistical analyses ...............................................................................................64
Chapter 4 Test-retest reliability of the soleus H-reflex in relation to joint positions and muscle force levels (Study I)..............................................66
4.1. Introduction .........................................................................................................67 4.2. Methods ...............................................................................................................68
4.2.1. Participants ...................................................................................................68 4.2.2. Experimental settings ...................................................................................69 4.2.3. Experimental procedures ..............................................................................70 4.2.4. Data analysis.................................................................................................72
4.2.5. Statistical analyses........................................................................................72 4.3. Results .................................................................................................................73
4.3.1. Reliability of the soleus H-reflex at different joint angles during rest .........73 4.3.2. Reliability of the soleus H-reflex during submaximal muscle contractions.74 4.3.3. Background EMG in the soleus and tibialis anterior muscles during submaximal voluntary contractions........................................................................74
4.4. Discussion............................................................................................................80
4.5. Conclusion ...........................................................................................................84 Chapter 5 Effects of joint position and muscle contraction intensity on soleus H-
reflex gain in young and older adults (Study II).....................................86 5.1. Introduction .........................................................................................................87 5.2. Methods ...............................................................................................................90
5.2.1. Participants ...................................................................................................90
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5.2.2. Experimental settings ...................................................................................91 5.2.3. Experimental procedures ..............................................................................91 5.2.4. Data analysis.................................................................................................92 5.2.5. Statistical analyses........................................................................................93
5.3. Results .................................................................................................................94 5.3.1. The soleus H-reflex gain ..............................................................................94 5.3.2. Background EMG in the soleus and tibialis anterior muscles......................94 5.3.3. Latency of the soleus H-reflex .....................................................................95 5.3.4. Duration of the soleus H-reflex ....................................................................95
5.4. Discussion..........................................................................................................100 5.4.1. Age-related changes in the soleus H-reflex gain ........................................100 5.4.2. Age-related changes in the soleus H-reflex latency and duration ..............102
5.5. Conclusion .........................................................................................................103 Chapter 6 Effect of ageing on soleus H-reflex modulation during shortening and
lengthening muscle actions in relation to postural control (Study III)104 6.1. Introduction .......................................................................................................105 6.2. Methods .............................................................................................................107
6.2.1. Participants .................................................................................................107 6.2.2. H-reflex test ................................................................................................107 6.2.3. Passive and active dynamic muscle actions ...............................................108 6.2.4. Postural tasks ..............................................................................................109 6.2.5. Data analysis...............................................................................................109 6.2.6. Statistical analyses......................................................................................110
6.3. Results ...............................................................................................................110 6.3.1. Dynamic muscle action test........................................................................110 6.3.2. The correlation between the maximal SOL H-reflex amplitude in the dynamic muscle action test and postural control tests..........................................111
6.4. Discussion..........................................................................................................118 6.4.1. Age-related changes in soleus H-reflex modulation during shortening and lengthening plantarflexors actions........................................................................118 6.4.2. Correlation of soleus H-reflex modulation between dynamic plantarflexion actions and postural tasks in young and older adults ...........................................121
6.5. Conclusion .........................................................................................................122 Chapter 7 Effect of 12 weeks Tai Chi training on soleus H-reflex and control of
static posture in older adults (Study IV) ...............................................123
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7.1. Introduction .......................................................................................................124 7.2. Methods .............................................................................................................127
7.2.1. Participants .................................................................................................127
7.2.2. Tai Chi training program ............................................................................128 7.2.3. H-reflex test ................................................................................................128
7.2.4. Static postural test.......................................................................................128 7.2.5. Experimental procedures ............................................................................129 7.2.6. Data analysis...............................................................................................129 7.2.7. Statistical analyses......................................................................................130
7.3. Results ...............................................................................................................130 7.3.1. Participants .................................................................................................130
7.3.2. Elimination of outlier data points ...............................................................130 7.3.3. H-reflex test ................................................................................................131
7.3.4. Centre of pressure measurement ................................................................131 7.4. Discussion..........................................................................................................136
7.4.1. Soleus H-reflex modulation........................................................................136 7.4.2. Static postural control.................................................................................137
7.4.3. The relationship between H-reflex modulation and postural control .........138 7.5. Conclusion .........................................................................................................139
Chapter 8 Summary, conclusions and implications ...........................................141 8.1. Summary of results ............................................................................................142
8.2. Conclusions .......................................................................................................144 8.3. Implications of the finding and future research.................................................146
References ...................................................................................................................150 Appendix A Information sheet ...............................................................................165 Appendix B Consent form ......................................................................................175 Appendix C Call for volunteers..............................................................................182 Appendix D Health status assessment prior to exercise testing ..........................188 Appendix E Tai Chi training program..................................................................197 Appendix F Original data .......................................................................................203
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List of Figures
Figure 2.1: Simplified illustration of Hoffmann reflex ..................................................19 Figure 2.2: Recruitment curve ........................................................................................24
Figure 2.3: A schematic diagram of spinal networks .....................................................34 Figure 2.4: A sketch of presynaptic inhibitory process. .................................................36 Figure 2.5: Illustration of reciprocal Ia inhibitory pathway. ..........................................38 Figure 2.6: The H-reflex modulation in the soleus (SOL) and medial gastrocnemius
(MG) muscles during task-dependent body sways......................................43 Figure 3.1: Locations of the stimulation and EMG electrodes.......................................56 Figure 3.2: Participants position in the isometric voluntary contraction test................58 Figure 3.3: The standardised upright position in the static postural tasks......................61 Figure 3.4: A schematic shows the data acquisition system. .........................................63 Figure 3.5: Raw EMG trace was used to quantify the SOL H-reflex parameters. .........63 Figure 4.1: Participants leg position in the soleus H-reflex test. ..................................70 Figure 4.2: The maximal soleus H-reflex amplitude recorded during rest, and 10%, 30%
and 50% maximal voluntary contraction at the neutral, plantarflexion, and dorsiflexion of ankle positions from a representative participant. ..............77
Figure 4.3: The soleus (A) and tibialis anterior (B) background EMG (bEMG) activity recorded during 10%, 30% and 50% maximal voluntary contractions at the neutral, plantarflexion and dorsiflexion positions in the Trial 1 (T1) and Trial 2 (T2). .................................................................................................79
Figure 5.1: Typical Hmax of the soleus H-reflex recorded during rest, and muscle contractions at 10%, 30% and 50% MVC at the neutral, plantarflexion and dorsiflexion of ankle positions in one young (left side) and one older (right side) participant. ..........................................................................................96
Figure 5.2: Influence of ageing on the soleus H-reflex gain during rest and submaximal muscle contractions when the ankle joint placed at neutral, plantarflexion and dorsiflexion positions............................................................................97
Figure 5.3: Background EMG of the soleus (A: young, C: older) and tibialis anterior (B: young, D: older) muscles during rest and soleus contractions at 10, 30 and 50% MVC in ankle joint positions of neutral, plantarflexion and dorsiflexion. .................................................................................................98
Figure 5.4: Latency (A) and duration (B) of maximal soleus H-reflex in the young (filled circles) and older groups (unfilled circles). ......................................99
xiv
Figure 6.1: H-reflex and M-wave recruitment curves during passive shortening (H-reflex: ; M-wave: ) and lengthening (H-reflex: ; M-wave: ) actions, and standing on stable surface with eyes opened (H-reflex: ; M-wave: ) from representative one young (A, B) and one older (C, D) participants, respectively. ...............................................................................................114
Figure 6.2: Representative raw EMG traces of the maximal soleus H-reflex during passive and active dynamic muscle activities and four different postural conditions from one young (solid lines: A, C) and one older (dotted lines: B, D) participants. ..........................................................................................115
Figure 6.3: The soleus Hmax to Mmax ratio during A) passive shortening and lengthening movements, and B) voluntary shortening and lengthening muscle contractions................................................................................................116
Figure 7.1: The SOL Hmax/Mmax ratio before and after 12-week Tai Chi training in the Training and Control groups......................................................................133
xv
List of Tables
Table 3.1: A summary of participants recruited in the four studies. .............................. 54 Table 3.2: Summary of the statistical analyses............................................................... 65 Table 4.1: Mean value, standard deviation (values in the brackets), intraclass correlation coefficients (ICC), and standard error of measurement (SEM) for the maximal voluntary contraction torque (MVC), the maximal amplitude of soleus H-reflex (Hmax), the maximal amplitude of soleus M-wave (Mmax), and the Hmax/Mmax ratio during rest and at three ankle joint positions in Trial 1 (T1) and Trial 2 (T2). ........................................... 75 Table 4.2: Mean value and standard deviation (in the brackets), intraclass correlation coefficients (ICC), and standard error of measurement (SEM) for the maximal amplitude of soleus H-reflex (Hmax) at three ankle positions during contractions at 10%, 30% and 50% maximal voluntary torque (MVC) in the Trial 1 (T1) and Trial 2 (T2). . 76 Table 6.1: Pearson correlation coefficients of the maximal soleus H-reflex amplitude between dynamic muscle activities and postural tasks, in the young and older adult groups. .......................................................................................................................... 117
Table 7.1: Comparison of physiological characteristics between the Tai Chi group and Control group prior to the 12 weeks of TC training. .................................................... 134
Table 7.2: Mean values and standard deviation of the mean displacement of COP values (anterior-posterior and medial-lateral directions) in four sensory conditions in the Tai Chi and Control groups before and after the 12-week training or control period. ....... 135
xvi
Abbreviation
A/D Analog to digital Ag/AgCl Silver silver chloride ANOVA Analysis of variance
bEMG Background electromyogram C-T Conditioning-test CNS Central nervous system COM Centre of mass
COP Centre of pressure COPA-P Centre of pressure movement in anterior and posterior direction COPM-L Centre of pressure movement in medial and lateral direction EEG Electroencephalogram EMG Electromyogram
EPSP Excitatory postsynaptic potential GABA Axo-axonal gamma-aminobutyric acids GVS Galvanic vestibular stimulation Hmax Maximal peak-to-peak amplitude of H-reflex ICC Intraclass coefficient correlation IPSP Inhibitory postsynaptic potential ISI Inter-stimulus interval MEPs Motor evoked potentials MG Medial gastrocnemius Mmax Maximal peak-to-peak amplitude of M-wave MVC Maximal voluntary contraction RMANOVA Repeated measures analysis of variance RMS Root mean square SC stable surface with eyes closed SD Standard deviation SEM Standard error of measurement SENIAM Surface EMG for a non-invasive assessment of muscles SO Stable surface with eyes open SOL Soleus muscle SOT Sensory organization test
TA Tibialis anterior muscle
xvii
TC Tai Chi
TES Transcranial electrical stimulation TMS Transcranial magnetic stimulation
UO Unstable surface with eyes open UC Unstable surface with eyes closed
xviii
Units of measurement
cm Centimetre Degree
/s Degree per second Hz Hertz
h Hour
Kg Kilogram
kHz Kilohertz
s Microsecond V Microvolt
mA Milliampere
mm Millimetre
ms Millisecond ms.cm-1 Millisecond per centimetre mV Millivolt
min Minute
N.m Newton meter
% Percentage s Second cm2 Square centimetre V Volt
1
Chapter 1 Introduction
2
1.1. Introduction
Humans adopt an upright posture in most physical activities. During standing, this
requires stabilisation of joint positions in multiple segments of the body in order to
maintain an appropriate posture. The ability to control the vertical projection of the
centre of mass (COM) relative to the base of support is defined as postural stability
(Horak, 2006). There are two major components to determine the postural stability
during standing: neural and musculoskeletal components (Horak, 2006). Neural
component refers to receiving the sensory information from the somatosensory,
vestibular and visual systems and sensorimotor processes that occur within the central
nervous system (CNS), whilst musculoskeletal component refers to muscular actions
resulting in biomechanical changes during postural control.
During bipedal standing, the body naturally oscillates in a model of inverted pendulum
(Winter, Patla, Prince, Ishac, & Gielo-Perczak, 1998). The body sways in the anterior-
posterior direction and medial-lateral directions. The kinematic action in control of
upright posture attempts to move the COM without changing the base of support (limits
of stability). When maintaining the upright posture the body sways at a mean frequency
of 1.3 Hz which corresponds to 2.6 times of postural reversion per second (Loram,
Maganaris, & Lakie, 2005b). The control of upright posture requires appropriate
strategies to maintain joint stability, mainly at ankle and hip joints (Horak, 2006). The
ankle strategy is used during standing on a stable surface with small amounts of body
sway, whereas the hip strategy is used during standing on a small base of support or an
unstable surface.
The body oscillations during standing are associated with changes in the ankle joints
within a range of 1.0-1.5 in the anterior-posterior direction (Gatev, Thomas, Kepple, &
3
Hallett, 1999). In this case, the ankle plantarflexors and dorsiflexors play an important
role in control of ankle movement and sway angle (Winter, Prince, Frank, Powell, &
Zabjek, 1996). Loram et al. (2005) utilising ultrasound imaging technique reported that
the contractile tissue of the plantarflexors is shortening during forward sway, whereas
that is lengthening during backward sway. The paradoxical muscle movements
observed in Loram et als study indicate that the plantarflexor muscles contract
concentrically, eccentrically, or even isometrically in order to maintain the position of
ankle joints.
The ankle muscle stiffness has an essential function in controlling upright posture
(Evans, Fellows, Rack, Ross, & Walters, 1983; Fitzpatrick, Gorman, Burke, &
Gandevia, 1992).Winter et al. (1998; 2001) proposed a model of stiffness control during
standing. In this model, neural mechanisms in control of ankle joint movements are
associated with neural inputs from multiple sources. The CNS regulates the tension of
ankle muscles in response to any change of ankle joint position, according to the
feedback of sensory information from the ankle joint (Winter, et al., 2001). The
feedback and feedforward controls of ankle joint movement regulated by the
supraspinal mechanisms coordinate the most joint motions in attempt to stabilising the
whole body position in the vertical alignment (Gatev et al., 1999). For example, ankle
strategy plays a crucial role to adjust standing posture during a small perturbation of
support translation in forward and backward direction. In contrast, the role of knee and
hip joint movements is minimal for postural control in this case.
Ageing is an inevitable part of the physiological process in human life. This process
results in deterioration of the neuromuscular functions and decreased physical capacity
at older ages (Nelson et al., 2007). Compared with young adults, older persons show
slower cognitive processing (Rozas, Juncos-Rabadan, & Gonzalez, 2008), motor
4
response generation (Kolev, Falkenstein, & Yordanova, 2006; Ward, 2006), nerve
conduction velocity (Rivner, Swift, & Malik, 2001), and electromechanical delay
(Mackey & Robinovitch, 2006; Zhou, Lawson, Morrison, & Fairweather, 1995), and
decreased muscle strength (Frontera et al., 2008) and power (McNeil, Vandervoort, &
Rice, 2007). As a result, older adults have less ability in performing motor tasks and
executing daily physical activities. Although the existing evidence indicates a
deterioration of neuromuscular function with ageing, older adults may adopt different
strategies in performing motor tasks as a result of compensatory adaptations (Earles,
Vardaxis, & Koceja, 2001; Scaglioni, Narici, Maffiuletti, Pensini, & Martin, 2003).
Older adults have shown an increase in postural sway during upright standing,
compared to young adults (Abrahamova & Hlavacka, 2008). The compromised postural
control is the result of age-related changes in sensorimotor (Sturnieks, St George, &
Lord, 2008) and muscular (Carrie et al., 2003) functions.
During standing, electromyographic activity (EMG) of the plantarflexors corresponds to
less than 5% of that during maximal voluntary isometric contractions (MVC). More
recently, Kouzaki and Sinohara (2010) demonstrated a significant correlation between
the coefficient of variation in the central of pressure displacement during standing and
coefficient of variation in force production during plantarflexion contractions around
5% MVC. The outcome of this study indicates that the neural control might have similar
characteristics with respect to control of ankle joint during isolated joint movement and
standing.
Motor control refers to sensorimotor performance during body movements (Latash,
Scholz, & Schoner, 2002). In the sensorimotor processes, the spinal motoneurons, such
as - and -motoneurons, are responsible for control of skeletal muscle activity. The
spinal motoneuron activity is regulated by integration of the descending inputs from the
5
supraspinal centres and the ascending inputs from the peripheral sensory receptors
(Hultborn, 2006). These neural inputs converging onto the spinal cord are major factors
to determine the firing rate and recruitment of spinal motoneurons. When a postsynaptic
membrane potential depolarizes (excitatory postsynaptic potentials, EPSP) to the
threshold level, an action potential is produced for discharge of the spinal motoneurons.
In contrast, a postsynaptic membrane potential can be reduced by inhibitory
postsynaptic potentials (IPSP), resulting in inhibition of the spinal motoneuron activity.
Variation in excitatory and inhibitory inputs can affect the recruitment of spinal
motoneurons. In human movement study, the Hoffmann reflex (H-reflex) has been
extensively used to evaluate the effectiveness of group Ia afferent inputs to excite the -
motoneuron during motor performance (Misiaszek, 2003).
The H-reflex is an electrically induced analogue of reflex and can be used to assess
group Ia excitatory effect on the -motoneuron activation (see detailed explanation in
Chapter 2 of this thesis). The H-reflex amplitude is influenced by neural inputs from
various afferent and efferent pathways, therefore it can be used as an indicator of the
outcomes of the motor output regulation through the supraspinal and spinal mechanisms
(Hultborn, 2006; Misiaszek, 2003). There has been evidence that the modulation of H-
reflex is task-dependent (Zehr, 2002). For example, the size of SOL H-reflex has been
found to vary upon ankle joint position (Guissard & Duchateau, 2006; Hwang, 2002),
muscle contraction intensity (Butler, Yue, & Darling, 1993; Stein, Estabrooks, McGie,
Roth, & Jones, 2007), and type of dynamic muscle actions (Duclay & Martin, 2005;
Duclay, Robbe, Pousson, & Martin, 2009). These observations can help us to
understand the motor output regulation during functional tasks. However, most of the
H-reflex studies in the current literature were based on young adults and may be
inappropriate to explain the H-reflex modulation in older adults due to ageing effects
6
(Earles, et al., 2001; Hortobagyi, del Olmo, & Rothwell, 2006; Kido, Tanaka, & Stein,
2004).
The amplitude of H-reflex increases proportionally with increased intensity of muscle
contraction (Stein, et al., 2007). The neural mechanism underlying the H-reflex
potentiation during muscle contraction has been suggested as increased neural drive
from the supraspinal levels (Nielsen, Petersen, Deuschl, & Ballegaard, 1993). The H-
reflex gain, as determined by a ratio the amplitude of H-reflex divided by the
background muscle activity, has been used to evaluate the contribution of Ia afferent
inputs to motoneuron activation during execution of motor tasks (Capaday, 1997). In the
previous studies, age-related changes in the SOL H-reflex have been reported during
10%, 20% and 30% of MVC at neutral ankle position (Angulo-Kinzler, Mynark, &
Koceja, 1998; Earles, et al., 2001). Young adults demonstrated that the SOL H-reflex
gain during submaximal voluntary muscle contractions was stronger in a lying prone
position than that at the same level of muscle contractions in a standing position. In
contrast, older adults showed no difference in the SOL H-reflex gain in the same testing
conditions (Angulo-Kinzler, et al., 1998). The difference of H-reflex gain between
young and older adults is suggested to be related to the age-related changes in
presynaptic inhibitory function (Angulo-Kinzler, et al., 1998; Earles, et al., 2001).
However, observing the H-reflex gain at the neutral ankle position may give insufficient
information in understanding the ankle strategy during postural control, because the
ankle joint position constantly changes during naturally sway of normal standing.
It has been suggested that the amplitude of SOL H-reflex increases during passive
shortening movement, compared with that during passive lengthening movement
(Nordlund, Thorstensson, & Cresswell, 2002; Pinniger, Nordlund, Steele, & Cresswell,
2001). The movement-related changes in the SOL H-reflex modulation have also been
7
observed during shortening and lengthening muscle contractions (Duclay & Martin,
2005; Duclay, et al., 2009). The differentiation of SOL H-reflex modulation during
dynamic muscle movement is mainly controlled by presynaptic inhibition via either the
central or peripheral mechanisms (Duchateau & Enoka, 2008). However, these findings
were based on young adults. It is unknown whether older adults may adopt similar
neural strategies in modulation of H-reflex during shortening and lengthening muscle
actions.
The SOL H-reflex modulation is task-dependent and is found to be related to the ability
to control upright posture (Taube, Gruber, & Gollhofer, 2008). Recently, a series of
studies conducted by Tokuno et al. (2007; 2008) suggested that the SOL H-reflex is
position- and direction-dependent during body sway in anterior-posterior direction.
They speculated that the specific characteristic of H-reflex is related to the direction of
postural sway when the triceps surae is eccentrically or concentrically contracting to
maintain upright standing. However, there is no information available to us to support
whether the SOL H-reflex modulation during upright standing is correlated to that
during dynamic muscle activities.
A very serious issue for older people is their balance control capacity. Statistically, one
in three community-dwelling older adults experiences at least one fall each year and
more than thirty percent of fallers require medical treatment after suffering fall injuries
(Sturnieks et al. 2010; Tinetti, Speechley, & Ginter, 1988). The implementation of
exercise interventions can prevent falls and reduce the risk of falling in older adults
(Sturnieks et al. 2010; Gardner, Buchner, Robertson, & Campbell, 2001). In recent
years, Tai Chi (TC) exercise has been found to be an effective exercise intervention and
widely utilised for improvement of balance control in older adults (Choi, Moon, & Song,
2005; Li et al., 2005; Lin, Hwang, Wang, Chang, & Wolf, 2006; Voukelatos, Cumming,
8
Lord, & Rissel, 2007; Zeeuwe et al., 2006). Older TC practitioners have shown better
postural control capacity than their non-TC-trained counterparts. It has been suggested
that adaptive changes after TC training in kinematic proprioception (Fong & Ng, 2006;
Li, Xu, & Hong, 2008; Tsang & Hui-Chan, 2003, 2004b), vestibular function (Tsang &
Hui-Chan, 2006; Tsang, Wong, Fu, & Hui-Chan, 2004), tactile acuity (Kerr et al., 2008)
and reaction time (Li, Xu, & Hong, 2009) are related to improvement of postural control.
Although these studies have shown evidence of neural plasticity to TC training, it is
unclear whether this neural adaptation has occurred at the spinal cord level or
supraspinal levels. The neural mechanisms at the spinal level play an important role in
regulation of spinal reflex during upright standing (Taube, Gruber, et al., 2008).
Measuring the H-reflex amplitude can provide information to understand the neural
plasticity at the spinal level (Taube, Gruber, et al., 2008). The outcome can help us to
understand whether the neural adaptations associated with TC training is relevant to the
spinal contribution.
To yield valid outcome of the H-reflex test, the method used to measure the H-reflex
needs to be reliable. In the previous studies, the test-retest reliability of H-reflex during
rest has been reported under a variety of experimental conditions (Clark, Cook, &
Ploutz-Snyder, 2007; Handcock, Williams, & Sullivan, 2001; Palmieri, Hoffman, &
Ingersoll, 2002). During static postural tasks, high reliability of SOL H-reflex test has
been reported, for example, the intraclass correlation coefficient (ICC) of 0.94 in supine
position and 0.80 in standing position was reported by Hopkins et al. (2000). Low ICC
value during upright standing is related to variability of H-reflex modulation due to
body sway. During voluntary muscle contractions, various neural mechanisms may be
involved in the SOL H-reflex modulation, depending upon the contraction intensity
(Stein, et al., 2007). However, there is no study that has reported the test-retest
reliability of H-reflex during voluntary muscle contraction. It has been demonstrated
9
that the amplitude of H-reflex is inconsistent during submaximal voluntary muscle
contractions even though under the consistent experimental conditions (Funase & Miles,
1999). Whether the variation of H-reflex is related to biological changes or a poor
reliability during repeated trials of H-reflex test has not yet been determined. This
information is important to advance current knowledge in understanding the reliability
of H-reflex test during more functional tasks.
The research focuses on the SOL H-reflex because the SOL muscle plays an important
role in maintaining upright posture during standing and the studies on the SOL H-reflex
modulation may help us to understand the neural mechanisms in postural control. In
light of the above, four studies were designed to answer the research questions. Study I
was designed to determine the test-retest reliability of SOL H-reflex during isometric
submaximal voluntary muscle contractions in neutral, plantarflexion, and dorsiflexion
positions and to establish reliable measurement of H-reflex test in our laboratory. Study
II was designed to investigate the influence of ageing on the SOL H-reflex modulation
during isometric submaximal voluntary muscle contractions in neutral, plantarflexion,
and dorsiflexion positions. Study III examined the influence of ageing on the SOL H-
reflex modulation during passive and active shortening and lengthening plantarflexors
actions. Study IV investigated the SOL H-reflex adaptation and its relation to static
postural control after 12 weeks of TC training in older adults.
1.2. Aims of the investigation
The objective of the research was to advance our knowledge in understanding the effect
of ageing on the SOL H-reflex modulation during different ankle joint positions, muscle
contraction intensities, dynamic muscle actions and static postural tasks. This research
10
also sought to investigate the effect of 12 weeks TC training on the SOL H-reflex
modulation and control of static posture in healthy older adults.
The specific aims of the studies are stated below.
Study I: Test-retest reliability of the SOL H-reflex
The aims of this study were:
1. To determine the test-retest reliability of SOL H-reflex at the ankle joint positions
of neutral (0), plantarflexion of 20 and dorsiflexion of 20.
2. To determine the test-retest reliability of the SOL H-reflex during rest and
voluntary contractions at 10%, 30% and 50% of MVC levels in the above-
mentioned three ankle joint positions.
The details of this study are described in Chapter 4.
Study II: Effects of joint position and muscle contraction intensity on soleus H-
reflex gain in young and older adults
The aim of the Study II was:
1. To examine the age-related differences in SOL H-reflex gain during submaximal
voluntary contractions at 10%, 30% and 50% MVC when the ankle joint was
placed at neutral (0), plantarflexion of 20 and dorsiflexion of 20.
The details of this study are described in Chapter 5.
Study III: Effect of ageing on soleus H-reflex modulation during shortening and
lengthening muscle actions in relation to postural control
11
The aims of this study were:
1. To determine age-related changes in the SOL H-reflex modulation during passive
and active shortening and lengthening muscle actions.
2. To determine the correlation of the SOL H-reflex modulations between shortening
and lengthening muscle actions and static postural tasks in young and older adults.
The details of this study are described in Chapter 6.
Study IV: Effect of 12 weeks Tai Chi training on soleus H-reflex and static
postural control in older adults
The aims of the Study IV were:
1. To determine the effect of 12-weeks TC training on the SOL H-reflex modulation
during static postural tasks in older adults.
2. To determine the effect of 12-weeks TC training on static postural control in older
adults.
The details of this study are described in Chapter 7.
1.3. Research hypotheses
The following research hypotheses were tested:
1. The test-retest reliability of the SOL H-reflex measurement is not affected by the
ankle joint position and muscle contraction intensity.
2. Ageing affects the SOL H-reflex gain during submaximal muscle contractions at
the neutral (0), plantarflexion 20 and dosiflexion 20 positions, because the age-
related differences of neural adaptation.
12
3. Ageing affects on the SOL H-reflex modulation during dynamic muscle actions
due to the age-related difference of neuromuscular adaptations.
4. The maximal amplitude of SOL H-reflex between dynamic muscle actions and
static postural tasks are correlated despite the ageing effect.
5. The maximal amplitude of SOL H-reflex is down-regulated after 12 weeks TC
training.
1.4. Significance of the research
An important aspect of postural control is that modulation of ankle muscle reflexes
plays a crucial role in maintaining upright posture. However, the characteristics of ankle
muscle reflexes during ankle joint movements and postural control is not well-
understood in older adults. This thesis aims to improve our fundamental knowledge in
understanding motor control strategies in older adults. The studies designed and
presented in this thesis were to investigate age-related changes in reflexive function of
the soleus muscle and neural adaptation to 12-week TC training in older adults. The
age-related differences of the SOL H-reflex modulation during different modes of ankle
muscle actions as well as the contribution of spinal adaptation caused by TC training
and its relation to control of static upright posture in older adults were examined. The
outcomes provided physiological evidence that advanced current
knowledge/understanding in improving balance control and reducing the risk of falls in
old population.
1.5. Study Limitations
1. This research was limited to investigations on the H-reflex modulation in the SOL
muscle. The outcomes may not be able to explain age-related changes in reflexive
function of other postural muscles, such as quadriceps, hamstrings or erector
13
spinae muscle groups, etc..
2. Due to the participants schedule and the availability of the research laboratories, it
was difficult to conduct the TC training experiments at the same time of the day.
Despite a controversial finding of the SOL H-reflex modulation during circadian
rhythm was reported in young adults (Guette, Gondin, & Martin, 2005; Lagerquist,
Zehr, Baldwin, Klakowicz, & Collins, 2006), it is not known whether the H-reflex
response of older adults could be affected by circadian variations.
3. The effects of TC training on H-reflex modulation and balance control in older
adults were limited to 12 weeks of intervention. The effects of longer-term TC
training cannot be addressed due to the limited duration of the Ph.D. candidature.
1.6. Delimitation
1. The participants recruited for this study were healthy young and older adults. The
explanation and implication of the outcomes were based on these populations.
2. This research examined H-reflex modulation when the body was in a steady
position. The outcomes of this study may not be applicable to H-reflex modulation
during dynamic activities (e.g., drop jumping, step climbing and walking).
1.7. Ethical approval
The research work presented in this thesis was conducted in compliance with the
Guidelines of the National Statement on Ethical Conduct in Research Involving
Humans (NHMRC). The criteria and standardisation of ethical aspects was supervised
by Southern Cross University Human Research Ethics Committee (EC00137). The
research was approved by the Human Research Ethics Committee of the University
(approval number ECN-08-092) and was performed in accordance with the Declaration
of Helsinki.
14
Chapter 2 Literature review
15
2.1. Introduction
The Hoffmann reflex, known as H-reflex, was originally described by a German
physician, Paul Hoffmann in 1910 (Hoffmann, 1910). The H-reflex test was extensively
used in the 1940s and early 1950s as a neurophysiological measurement and a non-
invasive technique to examine the influence of group Ia projection on the activation of
spinal -motoneurons (Magladery, Porter, Park, & Teasdall, 1951). Between the late
1950s and mid 1980s, this test was used to investigate the inhibitory or excitatory
influences of specific pathways on the activation of -motoneurons in conditioning
reflex protocols (Hultborn, 2006). More recently, the H-reflex test has been utilised in
studies on the role of Ia afferent spinal loop in various aspects of human movement, for
example, in relation to performance of functional tasks, such as single and multiple joint
movements, postural control, and locomotion (Zehr, 2002).
The -motoneuron activity is determined by summation of excitatory and inhibitory
inputs from afferent and efferent neural pathways (Pierrot-Deseilligny & Mazevet,
2000). It has been suggested that this reflex test can be used to investigate the effects of
neural inputs from either the peripheral sensory afferents or the descending pathways on
the spinal cord circuitry during motor performance (Hultborn, 2006). Action potentials
generated by group Ia afferent inputs, as indicated by the H-reflex response, is altered
dependently with respect to changes in body orientation (Knikou & Rymer, 2003) and
joint position (Alrowayeh, Sabbahi, & Etnyre, 2005; Chen et al., 2010; Hwang, 2002).
Recent studies have shown that the modulation of H-reflex response is highly correlated
to the phase and direction of postural sway and postural stability (Earles, Koceja, &
Shively, 2000; Taube, Leukel, & Gollhofer, 2008; Tokuno, et al., 2007; Tokuno, et al.,
2008). The size of H-reflex recorded from the triceps surae decreases in association with
16
increased body sway during bipedal stance. This relationship is more obvious during
postural perturbation (Earles, et al., 2000; Taube, Leukel, et al., 2008). In contrast, the
H-reflex amplitude is down-regulated in parallel with improvement of balance control
after one session (Mynark & Koceja, 2002) and repeated sessions of balance training
(Taube, Gruber, et al., 2008).
This review aims to provide an analysis of the current literature on the relationship
between the H-reflex modulation and control of upright standing posture for a better
understanding of the physiological mechanisms involved in postural control. The review
has three major sections. The first section discusses the physiology of H-reflex test and
technical considerations for its validity and reliability. The second section addresses the
supraspinal and spinal mechanisms related to control of posture. The third section
discusses the evidence presented in the literature on the relationship between the H-
reflex modulation (mainly the SOL H-reflex) and static postural control.
2.2. Validity and reliability of H-reflex measurement
2.2.1. H-wave and M-wave
The H-reflex is an electrical stimulation-induced analogue of reflex (Zehr, 2002). To
elicit the H-reflex, a percutaneous electrical stimulation is delivered to a peripheral
nerve branch which consists of mixed sensory and motor nerve fibres. When
depolarization of the nerve fibres reaches the threshold level, action potentials are
evoked and propagate on the nerve fibres in both the ascending and descending
directions. Subsequently, two types of compound muscle action potentials, M-wave and
H-wave, can be recorded from the skeletal muscle innervated by these nerve fibres.
17
The M-wave is recorded at the muscle as the result of the evoked action potential
travelling along the -motoneuron axons from the location of the electrical stimulation
to the muscle [response 1 in Figure 2.1 (Aagaard, Simonsen, Andersen, Magnusson, &
Dyhre-Poulsen, 2002)]. The M-wave amplitude reflects the number of the -
motoneuron axons being activated simultaneously (Tucker, et al., 2005). Under the
same stimulation intensity and testing conditions, this orthodromic action potential
should have a consistent amplitude, because it is determined by the physiological
characteristics of the efferent nerve fibres, neuromuscular junction and muscle fibres,
and is not affected by the sensory inputs and the spinal mechanisms (Frigon, Carroll,
Jones, Zehr, & Collins, 2007). However, the magnitude of M-wave may vary during
movements. The variations in the M-wave size may be caused by changes in muscle
fibre length, the distance between muscle fibres and EMG electrodes, and the spatial
relationship between the nerve and stimulation electrodes during movements (Tucker, et
al., 2005). For example, changes in joint position and level of muscle contraction can
alter action potential propagation along the sarcolemma therefore the size and duration
of M-wave response are changed (Frigon, et al., 2007).
From the location of the electric stimulation, action potentials also travel on the afferent
fibres, particularly the group Ia fibres, to the spinal motoneuron pool, that may
subsequently induce an H-wave (response 2 in Figure 2.1). If sufficient
neurotransmitters are released from the Ia afferent terminals, the -motoneurons will
respond with EPSP. Subsequently, an action potential may be generated on the
motoneuron axon if the EPSP reaches the excitation threshold. The action potential
generated by the -motoneuron propagates along the efferent motor nerve fibre to the
neuromuscular junction (response 3 in Figure 2.1), leading to an action potential on the
muscle fibres it innervates (H-wave). The H-wave recorded at the muscle is the summed
18
action potentials of different motor units, therefore its amplitude may vary depending on
the excitability of individual motoneurons in the -motoneuron pool (Misiaszek, 2003).
The sensory Ia fibres are normally larger, therefore have a lower excitation threshold
than the motor fibres (Panizza et al., 1998). At low stimulation intensities action
potentials are elicited only on the sensory Ia fibres, therefore the H-wave may be
recorded while the M-wave is absent. When the stimulation intensity is high enough to
activate the motor fibres, the evoked action potential on the -motoneuron axons will
travel in both ascending and descending directions from the location of the stimulation.
The ascending (antidromic) action potential on the -motoneuron axons (response 1* in
Figure 2.1) collides with the descending action potential from the spinal cord on the
same axons (response 3 in Figure 2.1). Thus, the H-wave may become smaller or even
disappear with increased stimulation intensity. In contrast, the descending (orthodromic)
action potential on the -motoneuron axons travels from the location of the stimulation
to the muscle (response 1 in Figure 2.1) and results in the M-wave. The amplitude of the
M-wave is getting larger with progressively increased stimulation intensity until the
maximal level (Mmax) is reached (Pierrot-Deseilligny & Mazevet, 2000). With a given
stimulation intensity, the amplitude of the H-wave is a valid indication of the Ia
excitatory effect on the target motoneurons (Pierrot-Deseilligny & Mazevet, 2000).
19
Figure 2.1: Simplified illustration of Hoffmann reflex [adopted from Aaggard, et al. (2002)]. Low intensity electrical stimulation elicits the H-wave (the second compound EMG wave shown in the EMG amplifier), whereas high intensity electrical stimulation elicits the M-wave (the first compound EMG wave). Because the axon diameter of the sensory Ia fibres is relatively larger, their excitation threshold is relatively lower than other types of fibres. Therefore, low intensity stimulation only elicits action potential on the Ia afferent axons (response 2) but not on the efferent motor axons. The afferent action potential induces EPSP on the spinal -motoneurons and may elicit an action potential on the -motoneuron axons that propagates to the target muscle (response 3). This response recorded from the muscle is the H-reflex wave. When the stimulation intensity increases gradually to the threshold level of the -motoneuron axons, action potential is produced on the axons at the site of stimulation and travels toward both the muscle (response 1) and the spinal cord (response 1*). The orthodromic action potential (response 1) propagates to the muscle that results in the M-wave, while the antidromic action potential (response 1*) travels toward the spinal cord and may collide with the action potential coming from the -motoneurons (response 3). The latter behaviour may cause partial or complete cancellation of the H-wave.
2.2.2. Reliability of H-reflex
The reliability of the H-reflex test has been examined in different age populations
(Mynark, 2005), and under various experimental conditions, for instance, in different
body positions (Ali & Sabbahi, 2001; Hopkins, et al., 2000), with and over different
time periods (Clark, et al., 2007), with and without conditioning-test (C-T) stimulations
(Earles, Morris, Peng, & Koceja, 2002), and in the upper (Jaberzadeh, Scutter, Warden-
H-wave pathway
M-wave pathway
The material has been removed
20
Flood, & Nazeran, 2004; Stowe, Hughes-Zahner, Stylianou, Schindler-Ivens, & Quaney,
2008) and lower (Palmieri, et al., 2002) limb muscles. In general, these investigations
have indicated that the H-reflex test is a highly reliable assessment in repeated tests. For
example, intraclass correlation coefficients (ICC) in the measurement of peak-to-peak
amplitude of the H-wave over two consecutive days have been reported as 0.99 in the
SOL, 0.99 in the peroneal, and 0.86 in the tibialis anterior (TA) muscles (Palmieri, et al.,
2002).
2.2.3. Methodological concerns in H-reflex assessment
Assessment of the H-reflex requires delivery of electrical stimulation to a peripheral
nerve and recording of action potentials (EMG) from a muscle innervated by the nerve
(Palmieri, Ingersoll, & Hoffman, 2004). The methodological considerations typically
include the configuration, placement and type of the stimulation electrodes, intensity
and duration of the stimuli, inter-stimuli interval (ISI), EMG configuration and location
of electrodes (Palmieri, et al., 2004; Pierrot-Deseilligny & Mazevet, 2000; Tucker, et al.,
2005). Furthermore, the potential effect of fatigue should also be considered in
experimental protocols that involve repeated high intensity muscle contractions or
prolonged testing time (Cresswell & Lscher, 2000; Rupp, Girard, & Perrey, 2010;
Walton, Kuchinad, Ivanova, & Garland, 2002).
Configuration and placement of stimulation electrodes
The H-reflex can be elicited using either unipolar or bipolar stimulation configuration.
The unipolar stimulation requires applying the electrical current to a location on a large
nerve trunk (Pierrot-Deseilligny & Mazevet, 2000). The cathode is placed over a mixed
peripheral nerve, for example, on the tibialis nerve (e.g. on the popliteal fossa) for
21
eliciting the H-reflex in the calf muscles, while the anode is placed on the opposite side
of the limb (e.g. on the patella) (Pierrot-Deseilligny & Mazevet, 2000).
In contrast, the bipolar stimulation is used at a more focused location for stimulation on
the nerve of interest (Palmieri, et al., 2004). Both the cathode and anode are placed on
the same nerve, for instance, on the median nerve for testing the H-reflex of the flexor
carpi radialis (Stowe, et al., 2008). In order to maintain the quality of electrical
stimulation, it is suggested that the stimulation electrodes are secured on the skin by
applying a rubber strap or elastic bandage (Capaday, 1997; Sefton, Hicks-Little, Koceja,
& Cordova, 2007).
Types of stimulation electrodes
It is known that the electrode-skin impedance is affected by the material utilised for
making the stimulation electrodes, which may influence electrical current delivered to
the tissue (Capaday, 1997). However, there is little discussion in the literature on the
optimal material of stimulation electrodes (Pierrot-Deseilligny & Mazevet, 2000;
Tucker, et al., 2005). According to a survey conducted by a European biomedical
research organization, the Surface EMG for a Non-invasive Assessment of Muscles
(SENIAM), the most common material utilised to make the electrodes is Ag/AgCl
(Hermens, Freriks, Disselhorst-Klug, & Rau, 2000). For the size of the electrode, most
laboratories have used a relatively larger electrode for the anode, in the vicinity of 20
cm2, whereas the cathode is relatively smaller, around 2 cm2, using the unipolar
configuration (Tucker, et al., 2005). Capaday (1997) suggested that it was effective to
use Ag/AgCl electrode for the cathode and a large size of metal plate made of stainless
steel or brass for the anode electrode.
22
Stimulation parameters
The optimal intensity of electrical stimulation to induce the H-reflex response is
determined individually (Brinkworth, Tuncer, Tucker, Jaberzadeh, & Turker, 2007). It
is commonly accepted that it is essential to establish an M-wave and H-wave
recruitment curve for a proper investigation of the H-reflex (Pierrot-Deseilligny &
Mazevet, 2000). To establish a complete recruitment curve, the stimulation intensity is
progressively increased from the threshold of the H-wave to a level at which there is no
more increase in the M-wave amplitude. Through this process, the intensity that elicits
threshold response and that elicits the maximal amplitude of H-reflex (Hmax) and Mmax
for each individual can be identified [see Figure 2.2 (Palmieri, et al., 2004)]. Normally,
the amplitude of the Hmax recorded in the SOL muscle is on average approximately 60%
of the amplitude of the SOL Mmax during rest (Tucker & Trker, 2004).
In general, the stimulation intensity used to elicit the Mmax is higher than that to elicit
the H-reflex and Hmax (Capaday, 1997; Tucker & Trker, 2004). The Mmax represents
the activation of all the motor axons innervating the muscle (Pierrot-Deseilligny &
Mazevet, 2000). Once the recruitment curve is established, the Mmax can be used to
normalize the smaller M-waves associated with the H-reflex. The Mmax can also be used
to evaluate the proportion of the entire motoneuron pool activated by the group Ia
afferent inputs by calculation of Hmax/Mmax ratio (Pierrot-Deseilligny & Mazevet, 2000).
In order to avoid any potential systematic changes that affect all parameters in the trials,
it is recommended to record the Mmax under the respective testing conditions as a
reference (Tucker & Turker, 2007).
There has been no common recommendation on the optimal stimulation intensity that is
normalized to the Mmax or Hmax to elicit the H-reflex. Because the M-wave is not
affected by the spinal mechanisms, stimulation intensity at a low percentage of Mmax is
23
commonly used to ensure consistency of stimulation intensity. As illustrated in Figure
2.2, the Hmax usually occurs in company with a small M-wave. However, the threshold
of sensory Ia afferent and efferent motor axons varies individually and is affected by
age (Stein & Thompson, 2006). Thus, it is suggested that the optimal stimulation should
induce the Hmax or an H-wave that is companied by an M-wave at 10 - 25% of the Mmax
throughout the experiment (Palmieri, et al., 2004).
24
0
1
2
3
4
0 1 2 3 4 5 6 7
Stimulus intensity
Am
plitu
de (m
V)
H-reflexM-wave
Figure 2.2: Recruitment curve [adapted from Palmieri, et al. (2004)]. The stimulus intensity is gradually increased from 1 to 7 (arbitrary unit). The H-reflex wave appears first at lower intensities. The Hmax that occurs at intensity 3 is accompanied with a small M-wave. With further increase of intensity, the size of M-wave increases accordingly and the size of H-reflex decreases. When the maximum amplitude of M-wave is reached, the H-reflex ultimately vanishes.
The commonly used stimulation duration is in the range of 0.5 (Capaday, 1997) to 1.0
ms (Pierrot-Deseilligny & Mazevet, 2000) in H-reflex studies, based on the large time
constant of the sensory nerve fibres (Kiernan, Lin, & Burke, 2004; Lin, Chan, Pierrot-
Deseilligny, & Burke, 2002). Recently, Lagerquist and Collins (2008) compared the
H/M recruitment curves established by short (0.05 and 0.2 ms) and long (0.5 and 1.0 ms)
pulse durations. A left shift of the recruitment curve was demonstrated when long
duration pulses were used. The size of the H-reflex was about 30% of the size of the
Mmax during trials with 1.0 ms pulse duration, and 10% of the Mmax during trials with
0.05 ms pulse duration when the M-wave associated with the H-reflex was controlled at
5% of the Mmax. However, this study showed no significant differences in the values of
Hmax, Mmax, and Hmax/Mmax ratio despite the variations in pulse parameters.
The material has been removed
25
The ISI is another parameter that should be considered. The size of H-reflex in response
to repeated stimuli depends upon refractory period of group Ia fibre (Capaday, 1997;
Voigt & Sinkjaer, 1998). Short ISI may diminish the amount of synaptic
neurotransmitters released to the -motoneurons, leading to a reduction of the H-reflex
amplitude, which is known as postactivation depression (Hultborn et al., 1996). It has
been reported that the effect of postactivation depression induced by preceding
electrical stimulation persists for around 8 s (Misiaszek, 2003). The optimal ISI is
therefore recommended for at least 10 s to avoid possible influence of the postactivation
depression (Palmieri, et al., 2004). Furthermore, a randomized stimulus interval is
suggested to minimise the effect of anticipation (Hultborn, et al., 1996; Mynark, 2005;
Mynark & Koceja, 2002; Schieppati, Nardone, Siliotto, & Grasso, 1995; Stein, et al.,
2007).
EMG configuration and electrode location
It is well known that the M-wave and H-reflex waveforms can be affected by recording
techniques, such as configuration and location of the EMG electrodes (Tucker, et al.,
2005; Zehr, 2002).
Bipolar configuration with the surface electrodes placed over muscle belly is most
commonly used for recording H-reflex (Pierrot-Deseilligny & Mazevet, 2000). The
advantage of bipolar configuration is that common noise signals recorded by the two
electrodes can be reduced by cancellation (Tucker, et al., 2005). However, the
disadvantage of bipolar configuration is that a potential risk of crosstalk between tested
muscle and adjacent muscles may occur if the size of the electrodes and inter-electrode
distance are too large (Beck et al., 2005). To minimise this potential problem, it is
suggested that the electrode size be around 1 cm in diameter and the optimal inter-
electrode distance be 2 cm for recording EMG on large muscles (Hermens, et al., 2000).
26
In contrast, the monopolar configuration consists of one active electrode placed over the
mid portion of muscle bully and one reference electrode placed over the muscle tendon
(Pierrot-Deseilligny & Mazevet, 2000). The inter-electrode distance is not a major
concern in monopolar configuration (Tucker & Turker, 2005). However, the
disadvantage is an inferior noise-to-signal ratio and the potential contribution of
crosstalk between tested muscle and adjacent muscles (Tucker, et al., 2005).
For obtaining reliable EMG recording, the location for EMG electrode placement
should be consistently determined for repeated testing. (Rainoldi, Melchiorri, & Caruso,
2004). The electrodes should not be placed over the motor point of the muscle because
it may alter the amplitude of EMG signals (Mesin, Merletti, & Rainoldi, 2009).
Hermens et al. (2000) have recommended that the proper location should be at midway
between the innervation zone and the insertion of the muscle. Zehr (2002) has
summarized the recommended electrode locations for recording H-reflex on nine upper
limb muscles and seven lower limb muscles.
Influence of fatigue
It is understood that muscle fatigue may alter motor unit recruitment and firing
frequency that can be detected by surface EMG during neuromuscular tests (Cifrek,
Medved, Tonkovi, & Ostoji, 2009). However, the potential influence of muscle
fatigue on the H-reflex is rarely addressed in the literature. This may be due to
controversial findings of the H-reflex modulation in relation to fatiguing exercise
protocols (Cresswell & Lscher, 2000; Rupp, et al., 2010; Walton, et al., 2002).
Nevertheless, caution should be taken that experimental conditions, such as high
intensity of muscle activities, long duration of experiments, and repeated application of
electrical stimulation, might lead to muscle fatigue that may affect the outcomes of H-
reflex tests.
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A recent study demonstrated that constant intensity of electrical stimulation used
throughout the experiment can lead to invalidation of the H-reflex and M-wave results if
muscle fatigue occurs (Rupp, et al., 2010). This study suggested that a re-determined
recruitment curve established by fewer numbers of electrical stimulation is helpful for
validation of the H-reflex parameters during the recovery period after an exhaustive
muscle testing protocol. However, the practicality of such a recommendation is still to
be revealed.
2.2.4. Limitations of H-reflex test
It should be noted that the H-reflex test is not a robust measurement. It could result in a
misinterpretation if the researchers neglected the physiological characteristics of the H-
reflex. There are several limitations that should be emphasized when the H-reflex test is
utilised.
First, it is important to bear in mind that the spinal cord circuitry is oligosynpatic
(Pierrot-Deseilligny & Burke, 2005). Any neural input from the supraspinal and
peripheral pathways can potentially influence the H-reflex modulation through either
direct regulation of the motoneuron membrane potential or indirect regulation of
interneuronal circuitry (Misiaszek, 2003). The participants physiological and
psychological status during the experiment can affect the H-reflex results. For example,
it has been demonstrated that postural anxiety can depress the H-reflex modulation
(Sibley, Carpenter, Perry, & Frank, 2007).
Secondly, even under consistent experimental conditions, the H-reflex amplitude is
fractal and may vary temporally in time (Nozaki, Nakazawa, & Yamamoto, 1995). It is
necessary to normalize the H-reflex response to either the Mmax or controlled H-reflex
for appropriate interpretation of the H-reflex result and minimizing inter- and intra-
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subject variability. To do so, it is necessary to apply extra electrical stimulations under
the respective experimental conditions that may cause discomfort to some individuals.
Thirdly, the H-reflex response may not be observed in all experimental trials for all
participants. It is possible that the H-reflex test is unsuccessful in a small proportion of a
healthy population under some experimental conditions. Unpublished observation in our
laboratory found that the SOL H-reflex response was present during passive shortening
movement but was absent during passive lengthening movement in a small number of
older adults. The mechanisms for the absence of H-reflex response during lengthening
plantarflexors muscle activity are unclear, but it is speculated to be related to quiescence
of muscle spindle activity. It has been suggested that the failure of H-reflex elicitation in
the older population might be due to age-related spinal stenosis (Egli et al., 2007).
In summary, H-reflex is a short-latency reflex which has been utilised to examine the
effects of Ia afferent inputs on the -motoneuron activation. High test-retest reliability
of H-reflex has been reported in the literature. The size of the H-wave can be affected
by recording methods and fatigue. Therefore, both technical and physiological factors
should be carefully considered for valid measurement of the H-reflex response.
2.3. Control of posture
The neural strategies involved in postural control are complex but all relate to the
interactions between sensory and motor processes at the supraspinal and spinal levels.
2.3.1. Sensory inputs
Somatosensory inputs
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Somatosensory cue refers to proprioceptive and cutaneous sensations. Muscle spindles,
Golgi tendon organs and joint receptors are sensory sources of proprioception which
detect body displacement in relation to changes in muscle length and joint movement
(Shaffer & Harrison, 2007). The cutaneous receptors include nociceptors and thermal
receptors that detect conditions of cutaneous and subcutaneous tissues, such as pressure,
mechanical stimuli, temperature and pain (Sayenko et al., 2009; Shaffer & Harrison,
2007). Somatosensory feedback is essential in execution of motor tasks (Brooke & Zehr,
2006) including adjustment of posture during standing (Horak, Earhart, & Dietz, 2001),
particularly when visual and vestibular inputs are restricted (Winter, Allen, & Proske,
2005). For example, sensory information from the cutaneous receptors can identify
slight changes in ankle displacements (Meyer, Oddsson, & De Luca, 2004). An increase
in the afferent flow from the cutaneous receptors occurs to mediate postural reflexes
when there is an increased external perturbation (McIlroy et al., 2003). A recent study
(Sayenko, et al., 2009) demonstrated that cutaneous afferents activated from different
locations on the sole of the foot resulted in alterations of the H-reflex modulation. For
example, a conditioning stimulation applied to the metatarsal region led to inhibition of
the SOL H-reflex response, whereas a conditioning stimulation delivered to the heel
region facilitated the SOL H-reflex response.
Visual inputs
Vision provides a reliable source of sensory information for the CNS, including
contextual cues and trajectory movement of surrounding objects (Franklin, So, Burdet,
& Kawato, 2007). Through visual feedback, the supraspinal mechanisms can accurately
modify spatial orientation of the body to adapt postural behaviour and movement
(Duarte & Zatsiorsky, 2002; Wessberg & Vallbo, 1995). A recent study measuring the
H-reflex and changes of centre of pressure (COP) showed that an increase in postural
30
stability was associated with facilitation of the H-reflex amplitude when a visual target
was provided (Taube, Leukel, et al., 2008). In contrast, deprivation of visual feedback is
known to impair postural control (Hafstrm, Fransson, Karlberg, Ledin, & Magnusson,
2002; Hue et al., 2007; Van Deun et al., 2007) and to depress the H-reflex amplitude
(Earles, et al., 2000)
Vestibular inputs
The sensory receptors in the vestibular system are sensitive to any change in motion and
orientation of the head (Horak, Shupert, Dietz, & Horstmann, 1994). When the head
position changes, vestibular sensory signals are elicited by the receptors in the otoliths
organ and semicircular canals and contribute to the perception of body position for
spatial awareness. The functional roles of the vestibular system are complex but
generally related to facilitation of postural reflexes (Horak, et al., 2001). Vestibulospinal
inputs can directly affect the spinal motoneuron activation. This is shown in
experiments that use a galvanic vestibular stimulation (GVS) to elicit vestibular afferent
flows prior to an H-reflex stimulation (Kennedy, Cresswell, Chua, & Inglis, 2004). For
example, Lowrey and Bent (2009) utilised a bipolar binaural GVS 100 ms prior to
elicitation of the H-reflex response in the SOL muscle. The result showed that the SOL
H-reflex conditioned by GVS was increased about 20% compare to that without GVS.
Thus, it appears that the vestibular afferent is able to influence the SOL motoneuron
activity even in a prone position.
2.3.2. Supraspinal mechanisms
In the brain region, there are many sources of descending motor signals involving in
control of movement. This section f