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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,

iv

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

v

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.

vi

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.

viii

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.

ix

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

xi

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).

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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