THE EFFECT OF SEGMENTAL VIBRATION THERAPY ON COGNITIVE PROCESSING AND BALANCE IN OLDER ADULTS.

A dissertation submitted to Kent State University in partial fulfillment to the requirements for the degree of Doctor of Philosophy

by

Nhlalala Y.Z. Mavundza

May 2019 © Copyright All rights reserved

Dissertation written by

Nhlalala Y.Z. Mavundza

B.Sc., Stellenbosch University, 2011

B.Sc. (Honors), Stellenbosch University, 2012

Ph.D., Kent State University, 2019

Approved by

Angela L. Ridgel, Ph.D. , Chair, Doctoral Dissertation Committee

Eric M. Mintz, Ph.D. , Members, Doctoral Dissertation Committee

Colleen M. Novak, Ph.D.

Kimberly S. Peer, Ph.D.

Jacob E. Barkley, Ph.D.

Accepted by

Ernest J. Freeman, Ph.D._____, Director, School of Biomedical Sciences

James L. Blank, Ph.D. , Dean, College of Arts and Sciences

TABLE OF CONTENTS

TABLE OF CONTENTS ...... iii LIST OF FIGURES ...... v LIST OF TABLES ...... viii ACKNOWLEDGEMENTS ...... ix I. OVERVIEW CHAPTER ...... 1 Falls in older adults ...... 1 Risk Factors ...... 1 Assessment ...... 2 Postural balance ...... 4 Visual system ...... 5 Vestibular system ...... 6 Somatosensory system ...... 6 Muscular system ...... 7 Cognition ...... 9 Age related changes in postural balance ...... 10 Sensory Impairments ...... 10 Motor impairments ...... 13 Cognition and attention deficits ...... 14 Interventions for improving balance in older adults ...... 16 Aerobic Exercise ...... 16 Balance training ...... 17 Tai Chi...... 18 Resistance training ...... 18 Cognitive training ...... 19 Whole body vibration therapy ...... 20 Effects of whole body vibrations on muscular strength ...... 20 Effects of whole body vibrations on postural balance ...... 22 Effects of whole body vibrations on cognitive performance ...... 23 Segmental vibration therapy ...... 24 Rationale ...... 25 Objectives/Hypothesis ...... 26

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References ...... 27 II. THE EFFECT OF SEGMENTAL VIBRATION THERAPY ON MUSCLE ACTIVITY AND BALANCE PERFORMANCE UNDER DIFFERENT SENSORY CONDITIONS...... 50 Introduction ...... 50 Methods ...... 55 Results ...... 59 Discussion ...... 71 Conclusion ...... 74 References ...... 76 III. THE EFFECT OF SEGMENTAL VIBRATION THERAPY ON EXECUTIVE FUNCTION...... 83 Introduction ...... 83 Methods ...... 85 Result ...... 88 Discussion ...... 96 Conclusion ...... 99 References ...... 100 IV. THE EFFECT OF SEGMENTAL VIBRATION THERAPY ON DUAL TASKING POSTURAL BALANCE IN OLDER ADULTS...... 104 Introduction ...... 104 Methods ...... 108 Results ...... 112 Discussion ...... 132 Conclusion ...... 135 References ...... 136 V. SUMMARY CHAPTER ...... 142 References ...... 146 APPENDICES ...... 149 Appendix A: Effect of SVT on balance and muscle activity data tables. ... 150 Appendix B: Effect of SVT on Executive function data tables...... 152 Appendix C: Effect of SVT on dual-tasking postural balance data tables . 153

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LIST OF FIGURES

Figure 1. Box plot represents data for fall risk pre-post CON vs SVT...... 60

Figure 2. Box plot of m-CTSIB sway index scores CON vs SVT during the firm surface conditions...... 62

Figure 3. Box plot of m-CTSIB sway index scores CON vs SVT during the soft surface conditions ...... 63

Figure 4. Box-plots of soleus muscle activity CON vs SVT during the firm surface conditions...... 65

Figure 5. Box-plots of soleus muscle activity CON vs SVT during the soft surface conditions...... 66

Figure 6. Box-plot of lateral gastrocnemius muscle activity CON vs SVT during firm surface conditions...... 67

Figure 7. Box-plot of lateral gastrocnemius muscle activity CON vs SVT during soft surface conditions...... 68

Figure 8. Box-plot of tibialis anterior muscle activity CON vs SVT during firm surface conditions ...... 69

Figure 9. Box-plot of tibialis anterior muscle activity CON vs SVT during soft surface conditions ...... 70

Figure 10. Box plot represents data for attention and inhibition computed scores...... 90

Figure 11. Box plot represents data for attention and inhibition fully corrected

T- scores ...... 91

Figure 12. Box plot represents data for working memory raw scores...... 92

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Figure 13. Box plot represents data for working memory fully corrected T- scores...... 93

Figure 14. Box plot represents data for processing speed raw scores...... 94

Figure 15. Box plot represents data for processing speed fully corrected T- scores...... 95

Figure 16. Dual-tasking m-CTSIB sway index scores CON vs SVT during firm surface conditions...... 114

Figure 17. Dual-tasking m-CTSIB sway index scores CON vs SVT during soft surface conditions...... 115

Figure 18. Single-task vs dual-tasking m-CTSIB sway index scores CON vs

SVT during firm surface conditions...... 117

Figure 19. Single-task vs dual-tasking m-CTSIB sway index scores CON vs

SVT during soft surface conditions...... 118

Figure 20. Box-plots of the dual-tasking soleus muscle activity CON vs SVT during firm surface conditions ...... 120

Figure 21. Box-plots of the dual-tasking soleus muscle activity CON vs SVT during soft surface conditions...... 121

Figure 22. Box-plot of dual-tasking lateral gastrocnemius muscle activity CON vs SVT during firm surface conditions...... 122

Figure 23. Box-plot of dual-tasking lateral gastrocnemius muscle activity CON vs SVT during salt surface conditions...... 123

Figure 24. Box-plot of dual-tasking tibialis anterior muscle activity CON vs

SVT during firm surface conditions...... 124

Figure 25. Box-plot of dual-tasking tibialis anterior muscle activity CON vs

SVT during soft surface conditions...... 125

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Figure 26. Box plot of the dual-tasking motor cost CON vs SVT during firm surface conditions...... 127

Figure 27. Box plot of the dual-tasking motor cost CON vs SVT during soft surface conditions ...... 128

Figure 28. Box plot of the dual-tasking cognitive cost CON vs SVT during firm surface conditions...... 130

Figure 29. Box plot of the dual-tasking cognitive cost CON vs SVT during soft surface conditions...... 131

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LIST OF TABLES

Table 1. Demographic characteristics of participants in both groups for the balance assessment...... 59

Table 2. Demographic characteristics of participants in both groups for the executive function...... 89

Table 3. Demographic characteristics of participants in both groups fot the dual-tasking assessment...... 112

Table A. 1. m-CTSIB sway index scores ...... 150

Table A. 2. Muscle activity (as percentage of MVC) during each balance condition CON vs SVT...... 151

Table B. 1. Attention and Inhibition scores...... 152

Table B. 2. Working memory scores...... 152

Table B. 3. Processing speed scores...... 152

Table C. 1. Dual-task m-CTSIB sway index scores...... 153

Table C. 2. Single-task vs. Dual-task m-CTSIB change scores...... 153

Table C. 3. Muscle activity during dual-tasking m-CTSIB...... 154

Table C. 4. Dual-task motor cost (%)...... 155

Table C. 5. Dual-task cognitive cost (%)...... 155

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ACKNOWLEDGEMENTS

First, and most of all, I would like to thank God for the strength and ability to complete this dissertation and putting the right people in my path to guide me and support me. I would like to thank my advisor Dr. Angela Ridgel for her expertise, guidance, support and confidence in me and my work, especially during the challenging times. Her kindness and patience coupled with her expertise makes her an inspirational researcher. Thank you to my committee members, for their insightful knowledge and thoughtful feedback for this research. I would also like to thank the members of the Lab

(Department of Exercise Physiology) for their assistance with my research project.

Thank you to the Fulbright Foreign Student Program and the National

Research Foundation of South Africa for funding my Ph.D. studies in the

United States. I also owe so much gratitude to the Dr. Benjamin van Duuren grant for helping me fund my research study. Thank you to the participants who volunteered and took time from their schedule to participate in the research study.

Lastly, I would like to thank my family and friends for their support. My mom,

Thembani Lubisi for always motivating me and helping me find a positive outlook with everything. My sister, Ntwanano Mavundza for her inspiring words and a listening ear during the tough times. My brother, Tefo Lubisi for always being there to help me clear my mind and put a smile on my face.

Thank you to my extended family and friends for their support, encouragement and for making this journey a pleasure.

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I. OVERVIEW CHAPTER

Falls in older adults

Falls among older adults ≥65 years is the leading cause of fatal and non-fatal injuries (CDC, 2014). In 2014, approximately 27,000 older adults died from falls and 3.6 million were hospitalized (CDC, 2016). Non-fatal injuries from falls cause morbidity with decreased function and loss of independence

(Alamgir, 2012). This imposes a social and economic burden on the patients, their family and communities. In addition, people who fall are at a further risk for more falls and they often limit their activity which can lead to other health issues, including muscle weakness and disability. With the elderly population increasing worldwide and healthcare cost on the rise, it is estimated that by

2020 the annual cost for fall related injuries will reach $54.9 billion (Englander,

1996).

Risk Factors

Causes for falls in older adults and multifactorial and include extrinsic and individual intrinsic factors. Extrinsic risk factors are accidents or environmental related falls (Rubenstein, 2006). Older adults are more at risk for accidental falls in hazardous environments such as those with complex steps, slippery floors and cluttered surroundings. The risk is further increased when they live alone. Accidental fall risks are increased by individual intrinsic risk factors

1 such as comorbidities that can cause dizziness, confusion, physical weakness and loss of consciousness, changes in muscle strength, visual deficits and impaired balance (Quigley et. al., 2010).

Medical conditions associated with falls are neurological and musculoskeletal disorders, sensory abnormalities, cardiovascular diseases and chronic medical conditions (Rubenstein, 2006). Furthermore, all patients in a nursing home are considered to be at a considerable risk for falls (Moylan et.al.,

2007). Patients in a nursing home have lost most of their independence to take care of themselves due to ageing and/or illnesses. Furthermore, they may be at an increased risk for falls due to transient factors such as medication and room changes (Neutel et.al., 2002). Most of the risk factors can be modified to decrease the risk of fall, such as changing or limiting medication; prescribing glasses for visual impairment or making sure they have a clear walking space and rails for support; increasing physical activity and strength training for muscle weakness, gait and balance difficulties.

Assessment

A fall is defined as an unintentional position change that results in the person coming to rest from an upright standing position to the ground, floor or other lower surface (Moylan et.al., 2007). “Fall risk screening” and “fall risk assessment” are terms that are used interchangeably but they should be distinguished. Screening is the process of identifying the people at risk for falls and assessment is used to identify the factors that make the individual at risk or increases their risk of falling (Close and Lord, 2011). Older patients rarely report their falls due to not remembering, embarrassment, and fear for

2 loss of independence or acceptance of the declining health and mobility

(Moylan and Binder, 2007). Therefore, physicians should be alert for signs that indicate falls, such as bruises, changes in cognition, disturbances in gait or balance and personality changes (Moylan and Binder, 2007).

Rueangsirarak et al., 2009 developed a Risk Assessment Matrix (RAM) as a screening tool for falls in older adults. It takes into account the possibility/likelihood and severity factors for falls. The possibility/likelihood are determined by biomechanical factors such as base support, step length, swing phase and hip flexion (Rueangsirarak et. al., 2012). The severity factor considers the walking, type of work and exercise that the individual can do without personal assistance (Rueangsirarak et. al., 2012).

The most common fall risk assessment method is medical diagnosis of associated disorders and medical conditions. Medical conditions that occur with ageing may contribute to falls include neurological disorders (stroke,

Parkinson’s disease, dementia), musculoskeletal disorders (joint deformities, muscle weakness and osteoarthritis) and sensory abnormalities (visual and hearing impairments, peripheral neuropathy) (Moylan and Binder, 2007).

Additionally, medication used for chronic medical conditions such as benzodizepines, antidepressants, antipsychotics, muscle relaxants and cardiovascular medications have been associated with falls in older adults

(Moylan and Binder, 2007). Most of these medications are identified by the

Beers Criteria as inappropriate for the elderly due to longer lasting adverse effects such as prolonged sedation, weakness and confusion which may further increase their risk for falls (Frick et.al., 2003). This criteria is helpful to identify fall risk in individuals with the specific disorders and conditions.

3

However, this approach may not be ideal due to the varying severity of the specific medical condition between individuals. The better approach for fall risk assessment would be a physiological profile assessment that aims to identify impairments rather than the cause (Lord et al., 2003). Balance involves the integration of multiple systems including vision, vestibular function, reaction time, peripheral sensation and muscle force (Lord et.al.,

2003), so these systems may need to be assessed separately.

Postural balance

Humans have a challenge to our balance system due to the inherently unstable bipedal stance and the feet alternating contact with the ground during locomotion (Winter, 1995). Posture is the orientation of the body relative to the gravitational vector and is an angular measure from the vertical and balance is the dynamics of the body posture to prevent falls (Winter,

1995). The central nervous system (CNS) uses input from many physiological systems to maintain postural balance. The visual system detects head orientation relative to the visual world, the vestibular system detects deviations of head orientation from the earth’s vertical gravitational pull, and the somatosensory, motor and musculoskeletal systems provide feedback to the central nervous system about body position and determines leg orientation relative to the support surface (Peterka et. al, 2002 and Era et.al.,

1996). Thus, postural control involves the input of various sensory systems and when one system is removed or functionally inefficient, postural control is more challenging. In addition, most of these systems deteriorate with age (Hu

4 et.al., 1994 and Manchester et.al., 1989), therefore, older adults have more difficulty in maintaining balance compared to younger adults (Wollacott et. al.,

1990). Additionally, cognitive processes such as executive function and attention are required to maintain balance during gait and standing (Smith-

Ray et. al., 2013).

Visual system

Normal subjects derive one-third of the orientation information from the visual input during quiet standing (Peterka, 2002). The retina of the eye determines self-motion and movement of the surroundings. When these visual inputs are different, such as a subject viewing a moving visual scene, then postural stability is affected (Lestienne et al., 1977). Individuals with visual loss have a higher risk for falls due to their inability to coordinate and plan movements while responding to surrounding environmental hazards (Beuno-Cavanillas et. al., 2000). Visual impairment can be caused by conditions including presbyopia, cataracts, glaucoma and macular degeneration (Watson, 2009).

A study by Ray and colleagues (Ray, 2008) showed that subjects with vision loss had a decrease in postural stability, increased postural sway and that they used hip-strategy to maintain balance which further increases their fall risk compared to subjects with normal vision. Visual cognition also plays a role in postural balance. This includes visual attention, visual-spatial ability and visual processing (Reed-Jones et al., 2013). In a study by Broman and colleagues (2004), divided visual attention was shown to be a great predictor of obstacle collisions and loss of balance during walking more than visual acuity and cognition.

5

Vestibular system

The vestibular system has both sensory and motor functions in maintaining postural balance. For the sensory function, the vestibular apparatus in the inner ear conveys signal to the CNS about the body’s position and movement.

The semicircular canals relay information about the angular acceleration of the head while the saccules and utricle sense linear acceleration of the head

(Balaban and Thayer, 2001). When the visual and the somatosensory systems are intact during postural balance, the sensory function of the vestibular system plays a minor role. The input of the vestibular system to maintain postural balance is more dominant when the visual and somatosensory systems are providing conflicting inputs (Begbie, 1967). The motor function of the vestibular system controls muscular reflex activity that initiates and regulates muscle tone through reflexes relayed to the vestibular-nuclear complex located in the pons (Hobeika, 1999).

These nuclei are connected to the cerebellum and brainstem and play a significant role in regulating postural balance with the vestibule-spinal system

(Hobeika, 1999). In addition to detection of movement and orientation, the vestibulo-ocular reflex which helps maintain gaze for target fixation during unexpected head and body movements (Hobeika, 1999) and the vestibulospinal reflex helps to maintains posture by initiating body movements that aim to stabilize the head over the trunk (Horak, 1987). These reflex mechanisms are part of the physiological factors that help maintain normal postural balance.

Somatosensory system

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The somatosensory system contributes to postural balance with proprioceptive inputs that include cutaneous and joint signals from the limbs and the feet which give the perception of joint movement and position when standing on a firm surface (Peterka, 2002; Lephart et.al., 1997). Specialized proprioceptive receptors in muscle, joint capsules, ligaments and skin relay afferent neural signals to the central nervous system for neuromuscular control to maintain stance or gait (Lephart et. al., 1997). Muscle spindles and golgi tendon organs play an important role in providing inputs that help maintain postural balance. The muscle spindles are mechanoreceptors which are stimulated by changes in muscle length and velocity of contraction to determine the joint movement and position (Shaffer and Harrison, 2007). The muscle spindles also provide feedback signals that initiate reflex and voluntary movements that are required for stability (Gaerlan et al., 2012).

Golgi tendon organs are found at the muscle tendon interface and they are activated when slight changes in tensile force in the muscle occur. Golgi tendon organs relay signals that inhibit alpha motor neurons (Shaffer and

Harrison, 2007) to decrease the tension in the muscle and tendon (Gaerlan et al., 2012).

Muscular system

Low levels of muscular force are required to maintain posture and keep the center of mass over the base of support (Corbeil et al., 2003). Balance requires the activation of muscle in the limbs, neck and trunk (Ting and

MacPherson, 2005). During postural control, leg muscle activation and co- activation of antagonist muscles attached to the ankle, knee and hip joints have a stabilizing effect on short term postural sway (Nagai et.al., 2012 and

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Nashner et.al, 1977). Two postural movements that stabilize posture in humans is the ankle strategy and the hip-knee strategy (Nashner and

McCollum, 1985). The ankle strategy is the most commonly used and it shifts the body’s center of gravity by rotating at the ankle without moving the hip and knee joints. Similarly, the hip-knee strategy positions the body’s center of gravity by flexing and extending at the hips or knees (Horak et. al., 1989).

Normal, young adults maintain balance in a distal to proximal manner, where muscle responses of the ankle strategy are activated first followed by the hip- knee muscles. Manchester and colleagues (1989) reported that when there is a posterior sway the muscle sequence of activation to restore balance starts from the tibialis anterior to the quadriceps and then the abdominal muscles.

While anterior sway induces muscle activation of the gastrocnemius followed by the bicep femoris and paraspinal muscles. Hip strategy is normally used when the support surface is smaller than the foot and involves the activation of the same muscle as the ankle strategy but in the reversed order, proximal to distal muscle responses (Manchester et. al., 1989).

Foot muscles are responsible for balance-correcting responses and are recruited with increasing postural demands and are normally synergistic with lower leg muscles (Schieppati et al., 1994). Motor output of the postural control system relies on activation and co-activation of leg and foot muscle and the contractual force of the muscles. Muscular fatigue of the lower leg muscle and foot creates higher demands for postural control (Corbeil et al.,

2003) which increases the risk for falls.

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Cognition

Cognitive functions such as executive function and attention are required to maintain balance during gait and standing (Smith-Ray et. al., 2013). In a study by Shumway-Cook and colleagues (Shumway-Cook et al., 1997), elder people with a history of falls took longer to regain postural stability following a perturbation while performing a cognitive task. Postural balance during daily activity involves motor-cognitive tasks while receiving signals from the external environment (Wollesen and Voelcker-Rehage, 2014). This interaction is referred to as dual tasking. Dual tasking creates an additional challenge to the maintenance of postural balance because of the increased inputs from various sensory systems and limited attention capacity (Huxhold et.al., 2006;

Lajoie et.al., 1993; Pellecchia, 2005). Research studies have observed a compromise in postural control while subjects are performing a cognitive task with a challenging proprioceptive and/or sensory input condition such as when eyes are closed or standing on an unstable surface (Anderson et.al., 1998;

Condron and Hill, 2002; Maylor and Wing, 2002; Melzner et.al., 2001).

However, other research has indicated an improvement in postural control while performing a cognitive task (Brown et.al., 2002; Dault et.al., 2001; Riley et.al., 2003). Therefore, postural control can either improve or be attenuated depending on the cognitive demand and task (Huxhold et.al., 2006). Cognitive tasks that require input or response using systems or sensorimotor pathways not involved in normal postural control such as verbal response, additional movements and mathematical calculations can worsen the postural control task (Dault et. al., 2003; Yardley et.al., 1999). While cognitive tasks that provide additional input to sensory systems contributing to normal postural

9 balance, like visual fixation to a stimulus, can improve postural tasks

(Stoffregen et.al., 1999 and 2000). Cognitive training, as well as motor cognitive dual-task training, improves gait and balance in young and older adults (Li et. al., 2010; Smith-Ray et. al., 2013; Lindenberg et. al., 2000). The interventions and cognitive training improved cognitive function and,subsequently, balance by influencing executive function, specifically- visuospatial working memory, processing speed and inhibition (Smith-Ray et. al., 2013).

Age related changes in postural balance

There are various age-related changes in postural control systems that have been observed in older adults over 65 years old who have reported falls

(MacRae et. al., 1992). Postural dysfunction in older people can result from sensory and motor impairments caused by pathology or loss of function due to normal ageing. Dysfunctions in the central processing system that affect cognition and attention can also contribute to the decline in postural stability.

Sensory Impairments

Vision is one of the three reference systems including proprioception and vestibular function that play a role in postural control in older adults. Visual cues from the surroundings provide input about the body’s center of gravity to maintain postural balance. With increasing age, this visual reference is impaired due to poor depth perception, decrease in visual acuity and restriction of the visual field (Grossniklaus et al., 2013). Poor depth perception

10 alters sensitivity to anterior-posterior sway-induced changes and a restricted visual field reduces the sensitivity to movement (Stelmach and Worringham,

1985). The elderly are also susceptible to pathological conditions such as cataracts, glaucoma and macular degeneration, which can reduce vision, visual sensitivity and restrict visual fields (Cohen and Lessell, 1984; Nag and

Wadhwa, 2012). Older adults with presbyopia and who need to wear multifocal glasses have impaired depth perception and edge-contrast sensitivity, which makes it a challenge for them to use stairs and increases their fall risk (Lord et. al., 2002). Glaucoma affects approximately 2% of older adults (Anderson, 2009) and can damage the optic nerve resulting in blindness or loss of peripheral vision, which can increase the risk for falls

(Reed-Jones et. al., 2013). Additional conditions like cataracts and age- related macular degeneration can cause vision loss, blurry vision and distortion of straight lines (Horton, 2012), which makes it difficult for older adults to move around their environments or have postural instability and are more at risk for falls (Black et.al., 2008). Furthermore, these visual deficits may result in the central nervous system delaying the reaction time to assess the rate, direction, landing and surrounding environment during a fall.

The key role of the vestibular function is to maintain the neck and the head in an upright position through the vestibulospinal and vestibulorecticulospinal pathways (Stelmach and Worringham, 1985). Vestibular degeneration such as reduced vestibular hair cells in the labyrinth (Johnsson and Hawkins, 1972;

Rauch et al., 2001), Scarpa's ganglion cells (Richter, 1980) and eighth cranial nerve fibers, which is the vestibulocochlear nerve that transmits signals on sense of hearing and balance (Bergström, 1973), have been observed in the

11 elderly. A large study by Fife and Baloh et. al., 1993 found that one third of adults over the age of 70 have vestibular impairment (Shumway-Cook and

Woollacott, 2001; Rauch et al., 2001). In addition, the vestibule-ocular reflex, which helps maintain visual fixation that assist with postural balance during postural challenges, is impaired in older adults (Johnsson, 1971). Although the vestibular function is less amenable compared to the visual and proprioceptive inputs to experimental manipulation, there is some agreement that it plays a role in resolving conflicting information between the visual and proprioceptive systems.

Proprioception, perception of the body’s, joint’s and limb’s relative position, is detected by mechanoreceptors located in the joints, ligaments, muscles, tendons and skin. A decline in proprioception, specifically of the lower limb, has a strong association with balance deficits in the elderly (Woollacott et. al.,

1986; Manchester et. al., 1989). Proprioception decline in the elderly can result from changes in both the central and peripheral nervous system. Within the peripheral nervous system, mechanoreceptors undergo anatomical and physiological changes due to ageing (Shaffer and Harrison, 2007). Spindle fibers change in function caused by a decrease in sensitivity (Miwa et. al.,

1995), denervation due to muscle atrophy (Swash and Fox, 1972) and deterioration of the spinal presynaptic inhibition pathways (Burke et. al.,

1996). Additionally, changes in the central nervous system lead to a decline in proprioception with ageing. Proprioceptive processing in the ageing is affected by the deterioration in conductive function of somatosensory pathways

(Tanosake et. al., 1999), loss of grey matter in the postcentral gyrus (Quiton,

2007) and a decline in the number of neurons and receptors (Masliah et.al.,

12

1993; Pakkenberg and Gundersen, 1997). Furthermore, neurochemical changes of neurotransmitter systems in the ageing brain (Strong, 1998) affect the functionality of proprioception and other neural systems that play a role in postural control. These include deficits of the cholinergic and serotonergic systems in the cortex and hippocampus, which are collectively associated with cognitive decline in ageing (Strong, et.al., 1991; Nelson et.al., 1988).

Additionally, there has been an observed decrease in Dopamine D2 receptors in the caudate and putamen of older adults which is highly related to age- related decline in motor performance (Dekosky and Palmer, 1994; Volkow et.al., 1998).

Motor impairments

One of the major factors that affect postural control and balance in old age is the decrease in muscle strength of the leg and core muscles (Wollacott et. al.,

1990; Shumway-Cook and Woollacott, 2001). This change could be a result of pathology, medication, lack of physical activity or normal ageing. When postural balance is challenged by surface movements, individuals typically use the ankle strategy first for stability followed by the hip-knee strategy

(Woollacott, 1986). Therefore, the muscle response to maintain balance is organized from distal to proximal muscle groups. Older adults have shown to have the same muscle response organization, however, they have significantly slow onset latencies (Woollacott 1986) and use the hip-knee strategy more often than younger adults during small balance threats (Horak et.al., 1989; Manchester et.al., 1989). Furthermore, the increased risk of falls

13 in older adults has been observed to correlate with reduced knee extension strength (Lord et.al., 1994) and hip strength (Robbins et.al., 1989). Whipple and colleagues (1987) showed that lower body muscle strength, specifically the ankle dorsiflexors, was severely impaired in older adults with a history of falls who are living in nursing homes. These changes could contribute to the increase in co-activation of antagonist muscle observed in older adults (Nagai et.al., 2012), which stiffens the joints and reduces the degree of motion resulting in an increased susceptibility to falls.

During postural control, leg muscle activation and co-activation of antagonist muscles attached to the ankle, knee and hip joints have a stabilizing effect on short term postural sway (Nagai et.al., 2012 and Nashner et.al, 1977).

However, in older adults, there is a change in muscle activity that results in a further increase in activation and more co-activation of antagonist muscles which acts as a compensatory mechanism for the decrease in muscle strength and deterioration of other systems that contribute to postural control and balance (Nagai et.al., 2012, Maki, 1993 and Wollacott et.al, 1990;

Macaluso and De Vito, 2004). This change in muscle strength and activity contributes to the increased incidence of falls and susceptibility to fall injuries.

Cognition and attention deficits

With increasing age, cognitive function such as executive function and attention decline while motor tasks such as balance and walking become less automated and cognitively taxing (Schaefer and Schumacher, 2011). These changes result in older adults having difficulties to perform a physical task

14 while simultaneously completing a secondary cognitive task (Laessoe et. al.,

2008). Furthermore, older adults with cognitive impairments have an increased risk of falling (Herman et. al., 2010; Holtzer et. al., 2007). The dual tasking deficit that is observed in older adults may be caused by the degradation of prefrontal cognitive processes (Smith-Ray et. al., 2013).

Dual tasking postural control is understood to be based on three principles: 1) that there is a limited processing capacity in the CNS; 2) that a single task uses part of the capacity and 3) if two or more tasks share the same processing capacity then their performance is distributed (Kahneman, 1973;

Parasuraman, 1981). Various studies have indicated an age-related effect on the attentional demands of postural control during a cognitive task. In some studies the postural control was negatively affected by performing a concurrent cognitive task (Smolders et.al., 2010; Doumas et.al., 2009) and in others both the postural control and the cognitive task were negatively affected (Shumway-Cook and Woollacott, 2000; Doumas et.al., 2008). The declining effect on postural control is further attenuated when there are conflicting inputs from sensory-balance systems which will require the older subjects to make postural adjustments. Somatosensory challenges such as altering the support surface and visual input concurrently creates a deficit in dual tasking postural control in older adults compared to young adults

(Redfern et.al., 2001; Shumway-Cook and Woollacott, 2000; Shumway-Cook et.al., 1997; Doumas et.al., 2008; Lajoie et.al., 1993). This indicates a decrease in attention capacity required for dual task postural control in older adults.

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Interventions for improving balance in older adults

To improve balance and reduce falls in older adults the risk factors for falls must be modified. Most of the extrinsic factors such as environmental hazards can be modified and have been used as preventative strategies (Clemson et.al., 2008). However, some interventions have targeted intrinsic factors to improve vision, muscle strength and balance to prevent falls or reduce the rate of falls in older adults. Training interventions such as gait, balance and coordination tasks, strengthening exercises and general physical activity have been used and have shown a positive effect in improving balance (Howe et. al., 2011).

Aerobic Exercise

Physical activity is known to improve the quality of daily life and minimize physiological impairments that are associated with ageing. An active lifestyle in older adults has demonstrated improvements in musculoskeletal, cardiovascular and respiratory health (Intiso et.al., 2012). Walking in older adults has shown to be effective in preventing falls in older adults due to the increase in physical activity, improving walking performance and delaying immobility (Malatesta et.al., 2010; Picelli et. al., 2012; Okubo et.al., 2016).

Strengthening and improving function of lower leg muscles would help older adults to maintain balance and prevent falls. Aerobic dancing with a focus on lower body muscle strength has shown to improve balance and decrease fall risk in old adults (Shigematsu et. al., 2002). Furthermore, the use of exercise

16 stability balls could help train proprioceptive inputs to help older adults improve their balance during challenging postural balance (Schlicht, 2002).

Balance training

Balance training that incorporates dynamic or static balance tasks has been shown to improve balance in older adults (Madureira et. al., 2007, Wollacott et.al., 1993 and Seidler et. al., 1997, Ledin et.al., 1990). Multisensory balance training, a training method that incorporates the various sensory inputs

(proprioception, vestibular and visual) and their integration, has improved balance due to the training of sensory organization abilities which have shown to deteriorate with age (Wollacott et. al., 1993, Hu et. al., 1994 and

Kristinsdottir et. al., 2014). Additionally, balance training using virtual reality games which incorporates multisensory training have shown improved balance and increase adherence to the intervention due to increased engagement (Bieryla et. al., 2013; Merriman et. al., 2015; Tsang et. al., 2016).

A study by Nagai et.al., (2012) also indicated that the increase in muscle co- activation observed in older adults can be attenuated by balance training. The balance training consisted of alternating stances and weight shifting. Post intervention measurements showed an increase in agonist (soleus) muscle activity and a decrease in antagonist (tibialis anterior) muscle activity during a functional reach and a forward functional stability boundary.

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Tai Chi

Tai chi is a martial art balance-enhancing exercise that uses slow continuous rhythmic movements controlled by the individual over their base of support (Li et.al., 2004; Hackney and Earhart, 2008). Tai chi has been used as a nontraditional exercise method to improve functional balance and lower leg strength. It has been shown to improve postural stability in older adults (Tse and Bailey, 1992; Hong et.al., 2000; Li et.al., 2004; Li et.al., 2005) due to its characteristics of using different ranges of motion, which improve flexibility, various postural orientation positions with the body’s mass displacements over the base of support and for engaging abdominal and lower leg muscles

(Li et.al., 2004; Li et.al., 2005).

Resistance training

Resistance training exercise interventions are helpful as balance training for older adults because they strengthen the leg and core muscles to support balance. Studies show an increase in muscle strength as well as improvements in balance after strength plus balance training intervention (Orr et. al., 2006, Wolfson et. al., 1996 and Schlicht et. al., 2001). In addition, resistance training increased balance confidence that was not correlated to fall risk and physical abilities (Liu-Ambrose et. al., 2004). Other research has been focused on multi-dimensional exercises to improve physical activity, muscle strength and balance in older adults with improved outcomes (Judge et. al., 1993; Shumway-Cook et. al., 1997; Alsubiheen et. al., 2015). The use of multi-dimensional exercise interventions allows for the improvement of

18 several factors that contribute to postural balance. It also provides the training for different postural balance conditions which would require either one of the factors (muscle strength, aerobic capacity and sensory integration) to be dominant during challenging postural conditions that require dependence of either factor.

Cognitive training

Cognitive decline in the elderly has been shown to result in a deficit in motor cognitive dual task performances (Huxhold et. al., 2006; Lindenberger et. al.,

2000). Cognitive training is a behavioural strategy that has improved cognitive domains such as the speed of processing information, auditory speed and accuracy in the elderly (Willis et. al., 2006; Smith et. al., 2009). One of the main mechanisms of cognitive training is that it uses the brain’s plasticity and/or compensates for the declining function by relocating neurocognitive tasks to other related brain regions or over activating to make up for the deficiencies in normal processing networks (Reuter-Lorenz and Cappell,

2008; Smith et. al., 2009; Smith-Ray et. al., 2013). Most research has focused on dual task training, which has shown significant improvements of not only postural balance but also dual tasking postural control (Lindenberg et. al.,

2000; Pellecchia, 2005; Silsupadol et. al., 2006; Li et. al., 2010). Additionally, cognitive training has shown the potential to improve gait and balance by influencing executive functions such as visuospatial working memory, processing speed and inhibition (Smith-Ray et. al., 2013).

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Whole body vibration therapy

Another method of muscle training that is gaining popularity in various clinical settings is vibration therapy. Vibration therapy has typically been performed as whole body vibration (WBV) therapy that uses a vibrating platform of adjustable frequency (number of oscillations) and amplitude (displacement of the oscillations) where the user stands on the platform and receives several bouts of vibration exposure (Rauch, 2009). The frequency for vibration therapy can range from 5Hz to 50Hz and the amplitude from 0.05mm to an intensive 10mm (Rauch, 2009; Cochrane, 2011). Whole body vibrations have shown to increase oxygen consumption, muscle temperature (Cochrane et. al., 2008), skin blood flow (Lohman et. al., 2007) and muscle force and power

(Cardinale and Bosco, 2003; Rauch, 2009) immediately after therapy. The increase in force and power observed following acute vibration therapy is thought to be attributed to neural effects such as motor-unit recruitment, synchronization and co-contraction from the vibration stimuli (Cardinale and

Bosco, 2003; Cochrane, 2011). The vibration causes neuromuscular effects by stimulating muscle spindles of the somatosensory system which activate alpha-motor neurons to generate muscle contraction through a spinal reflex mechanism (Cardinale and Bosco, 2003; Gribble et. al., 2004; Cochrane er.al., 2011). Whole body vibration therapy may be an alternative intervention for older adults who are unable to perform the conventional exercise due to limited mobility, functional performance and pain.

Effects of whole body vibrations on muscular strength

20

Older adults have shown to have a decrease in muscle mass which results in reduced muscle strength and increased fall risk (Evans, 1995). Resistance training has been the preferred method of enhancing muscle strength and function (Hunter et. al., 2004). However, WBV has also shown to induce similar muscular effects by stimulating stretch reflexes and inducing muscle contraction (Rehn et. al., 2007; Cardinale and Lim, 2003). According to

Delecluse and colleagues (2003), whole body vibration has the potential to induce strength gain in the knee extensors to the same extent as moderate resistance training. WBV therapy improved knee extensor strength and posture stability in elderly adults (Zhang et. al., 2014 and Tankisheva et. al.,

2014) and young healthy subjects (Torvinen et. al., 2002).

The activation of muscle by WBV has been demonstrated by an increase in muscle electromyograph activity (Bosco et. al., 1999; Cardinale and Lim,

2003). Roelants and colleagues (2006) reported that WBV induced a greater activation of the gastrocnemius muscle compared to the rectus femoris, demonstrating a distal to proximal effect. Additionally, Rees and colleagues

(2008) showed that muscle strength gains following WBV training in older people was greater for the ankle plantar flexors compared to the knee and hip flexors and extensors. These observed results were due to the standing position of the subjects on the vibrating platform. It indicates that proximity of the muscle to the vibrating device influences its effect and this outcome can be used for a more targeted effect to improve postural balance in older adults.

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Effects of whole body vibrations on postural balance

WBV has also shown some effects on postural balance in the ageing population. Its effect on balance could be attributed to the improvement in muscle strength, neuromuscular changes and the stimulation of spinal reflexes. Various long term studies of older adults taking part in long term vibration training have shown an improvement in balance and muscle strength

(Tseng et.al., 2016; Bruyere et.al., 2005; Verschueren et. al., 2004). Some studies have indicated no effect of WBV on postural balance, especially when the balance test is standing on both feet (Bogaerts et. al., 2011; Marín et. al.,

2011). While other studies investigating the effect of WBV on single leg standing balance observed a significant improvement following the WBV training, indicating that single leg balance is more compromised in older adults (Jones et. al., 2013; Gusi et. al., 2006; Rees et. al., 2009).

One of the reasons for conflicting outcomes in WBV training is the use of different protocols. Long term training has shown improvements or no effects but single sessions or shorter training times did have an effect on balance. A single session of WBV therapy improved single leg balance but had no effect on joint leg position and mobility in older adults (Jones et. al., 2013). Torvinen and colleagues (2002) also observed an improvement in postural sway following only 4min of WBV training in younger adults. Furthermore, different studies have used different vibration frequencies and vibration devices. Lam et. al., (2012) reported that studies that used a vibration frequency range of

35-40Hz resulted in no effect of WBV on balance while those that used a range between 12.6Hz to 26Hz had significant results with the balance outcome.

22

Effects of whole body vibrations on cognitive performance

Studies have shown that cognitive training, as well as motor cognitive dual- task training improves gait and balance in young and older adults (Li et. al.,

2010; Smith-Ray et. al., 2013; Lindenberg et. al., 2000). The interventions and cognitive training improved cognitive functions and subsequently balance by influencing executive function- specifically visuospatial working memory, processing speed and inhibition (Smith-Ray et. al., 2013). Whole body vibration has beneficial physiological effects such as improved oxygen uptake, blood flow, muscle strength, balance and postural control (Cardinale & Bosco,

2003; Conchrane et. al., 2008). Animal studies provide evidence of improved maze learning and enhanced neuronal activity in mice following whole body vibration (Keijser et. al., 2011). WBV training has shown to improve cognitive function, particularly inhibitory control as a measure of attention, in adults with attention deficit hyperactivity disorder (ADHD) and healthy children

(Fuermaier et. al., 2014; den Heijer et. al., 2015).

The possible explanation for the effect of WBV on cognition is the neuroanatomic connection between the mechanoreceptor and cognitive regions in the brain (Regterschot et. al., 2014). WBV stimulates muscle spindles, as well as mechanoreceptors in the skin, which send afferent signals to the primary somatic sensory cortex (Rauch, 2009). The sensory cortex has direct and indirect connection to the prefrontal cortex, which plays a key role in cognitive function (Braak et. al., 1996; Smith and Jonides, 1999; Kolb and

Whishaw, 2009). Furthermore, the limbic system, which is important for learning and memory, provides an indirect pathway between the sensory region and the prefrontal area (Braak et. al., 1996). Therefore, the sensory

23 stimulation from the WBV could influence neural activity in the sensory cortex as well as other brain regions that play a role in cognition.

Segmental vibration therapy

Whole body vibrations may provide effective benefits without strenuous effort from the user. However, the vibrations are not directed to a specific muscle group and the stimuli is widespread unless dynamic movements of certain muscle groups are incorporated into the vibration protocol. Segmental vibration therapy (SVT) can be used to target specific muscle groups. The vibration can be directly targeted to a muscle group of interest, while the participants receiving vibration therapy can be in a seated position (Ridgel et. al., 2013; Peer et. al., 2009) and there will be minimum side effects such as dizziness and nausea, from stimulation of the whole body (Cronin et. al.,

2004). Additionally, the stimulus is directly applied to the region of interest and can be of a lower frequency than what is used for whole body vibration therapy and still have beneficial effects (Peer et. al., 2009).

According to Paoloni and colleagues (2014), segmental muscle vibration has shown to modulate muscle activity and induced a low degree of co-activation of antagonist muscles of the arm during a reaching movement. SVT has also been used to treat ankle sprains and hamstring injuries in healthy adults resulting in significant acute effects of improving flexibility and reducing perceived stiffness (Peer et. al., 2009). Additionally, SVT has been used as a therapy for post-stroke patients to improve motor function (Caliandro et. al.,

2012) and reduce spasticity of hemiplegic limbs (Noma et. al., 2009; 2012).

24

These effects of SVT on muscle activity provide a potential therapy for the age-related changes in muscle function, such as stiffness and flexibility, that affect postural balance in older adults.

The demonstrated link between balance, muscle strength, vibration therapy and cognition indicate the potential of a vibration therapy, specifically segmental vibration therapy (SVT), to improve balance through the physical stimulation that acts on muscle recruitment and muscle strength and also improve the executive function of cognitive function in older adults.

Rationale

The primary objective of this study is to determine if sessions of segmental vibration therapy improve dual tasking postural balance and cognition in older adults. The central hypothesis is that the vibration therapy will provide a sensory stimulation that acts on muscle spindles and mechanoreceptors that could stimulate neural activity of the leg muscle and the sensory cortex as well as other brain regions. Stimulating the muscle spindles activates stretch reflexes and induces muscle contractions to improve muscle strength (Rehn et. al., 2007; Cardinale and Lim, 2003). While stimulating mechanoreceptors stimulates the sensory cortex which has direct and indirect connection to the prefrontal cortex, which plays a key role in cognitive function (Braak et. al., 1996; Smith and Jonides, 1999; Kolb and Whishaw, 2009).

Thus, vibration therapy has the potential to improve muscle activity and executive function which could result in an improvement on postural balance during dual tasking in the older adults.

25

Objectives/Hypothesis

Our first aim is to determine the effect of SVT on muscle activity and balance during a balance task under different sensory conditions. We hypothesize that the segmental vibration therapy will improve balance during a double leg stance in different conditions that challenge sensory inputs which play a role in maintaining balance. Additionally, we hypothesize that the vibration therapy will elicit improved muscle activity in the leg muscles of older adults. The second aim is to determine the effect of SVT on executive function. The purpose of this aim will be to determine whether the segmental vibration therapy will improve executive function specifically, the speed of processing, visuospatial working memory and attention/inhibitory control in older adults. Our hypothesis is that three sessions of vibration therapy will improve executive function. Lastly, we would like to determine whether the SVT will improve dual tasking ability during a postural balance test. The purpose of this aim is to determine whether the combined effect of the segmental vibration on muscle activity and executive function will lead to an improvement in dual tasking postural control in older adults. Our hypothesis is that, following segmental vibration therapy, older adults will have improved performance during a dual task postural test.

26

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49

II. THE EFFECT OF SEGMENTAL VIBRATION THERAPY ON MUSCLE ACTIVITY AND BALANCE PERFORMANCE UNDER DIFFERENT SENSORY CONDITIONS.

Introduction

Falls among older adults above 65 years old is a leading cause of fatal and non-fatal injuries (Center of Disease Control, 2014). The causes of falls are multifactorial with extrinsic and intrinsic risk factors. Extrinsic risk factors are accidents or environmental related falls (Rubeinstein, 2006) and intrinsic risk factors can be physical weakness, confusion, comorbidities that cause dizziness, decreased muscle strength, visual deficit and impaired balance

(Quigley et, al., 2010). Impaired balance in the elderly can result from deterioration of sensory, motor and central processing systems, which all contribute to balance control (Sturnieks et, al., 2008).

Postural Balance

During standing, the central nervous system (CNS) uses inputs from various sensory systems to maintain postural balance. The visual system detects head orientation relative to the visual world. The vestibular system detects deviation in head orientation from the earth’s vertical gravitational pull and provides feedback to the CNS about body position relative to the support surface (Era et, al., 1996 and Peterka et. al., 2002). The proprioceptive system includes sensors in the joints, tendons and muscles that provide input on joint position, muscle force, muscle length and touch (Sturnieks et, al.,

50

2008). Proprioceptive input from the lower legs provides most of the input during quiet standing (Fitzpatrick & McCloskey, 1994 and Sturnieks et, al.,

2008). Muscle spindles and golgi tendon organs are the proprioceptive receptors that play an essential role in providing inputs that help maintain postural balance. The muscle spindles are mechanoreceptors which are stimulated by changes in muscle length and velocity of contraction to determine joint movement and position (Shaffer & Harrison, 2007). They also provide feedback signals that initiate reflexes and voluntary movements that are required for stability (Gaerlan et. al., 2012). Golgi tendon organs are found at the muscle tendon interface and are activated when there are slight changes in the tensile force of the muscle. These receptors relay signals that inhibit activation of alpha motor neurons, which decreases the tension in the muscle and tendon (Shaffer & Harrison, 2007 and Gaerlan et. al., 2012).

While proprioceptive input plays a major role in postural balance, muscle receptors provide primary sensory feedback during quiet standing

(Fitzpatrick & McCloskey, 1994). Low levels of muscle force are required to maintain posture and keep the center of mass over the base of support

(Corbeil et. al., 2003). During postural control while quietly standing, leg muscle activation and co-activation of antagonist muscles attached to the ankle, knee and hip joints have a stabilizing effect on short term postural sway

(Nashner et. al., 1977 and Nagai et. al., 2012). When the feet are placed side by side during quiet standing, the ankle strategy is the most commonly used to counter the anterior - posterior sway of the body (Nashner & McCollum,

1985; Horak et. al., 1989 and Winter, 1995). When the body sways in the

51 anterior direction, the muscles attached to the ankle, specifically the soleus and gastrocnemius (plantar flexors), activate to shift the body’s center of mass at the ankle without moving the hip and knee joints to stabilize the body

(Horak et. al., 1989 and Lakie et. al., 2003). Additionally, the tibialis anterior

(dorsiflexor) acts as a primary agonist to restabilize the body’s center of mass following a postural sway, but with less activation than the soleus (Di Giulio et. al., 2009).

Vibration therapy

To improve balance and reduce falls in older adults, the risk factors for falls must be minimized. Interventions that target intrinsic factors such as muscle strength and activity can be used with preventative strategies to reduce extrinsic risk factors. A method of muscle training that is gaining popularity in various clinical settings is vibration therapy. Vibration therapy has typically been performed as whole body vibration (WBV) therapy that uses a vibrating platform of adjustable frequency (number of oscillations) and amplitude

(displacement of the oscillations) where the user stands on the platform and receives several bouts of vibration exposure (Rauch, 2009). The frequency for vibration therapy can range from 5Hz to 50Hz and the amplitude from 0.05mm to an intensive 10mm (Rauch, 2009; Cochrane et.al., 2011). Whole body vibrations have shown to increase oxygen consumption, muscle temperature

(Cochrane et. al., 2008), skin blood flow (Lohman et. al., 2007) and muscle force and power immediately after therapy (Cardinale and Bosco, 2003;

Rauch, 2009). The increase in force and power observed following acute vibration therapy is thought to be attributed to neural effects such as motor-

52 unit recruitment, synchronization and co-contraction of the muscles as a result of the vibration stimuli (Cardinale and Bosco, 2003; Cochrane et.al., 2011).

Vibration stimulates muscle spindles of the somatosensory system which activate alpha-motor neurons to generate muscle contraction through a spinal reflex mechanism (Cardinale and Bosco, 2003; Gribble et. al., 2004;

Cochrane et.al., 2011). Older adults show decreases in proprioceptive sensitivity which may contribute to unstable balance.

Several long-term vibration studies of 6 -24 weeks with 3 vibration sessions per week in older adults have documented an improvement in balance and muscle strength (Tseng et.al., 2016; Bruyere et.al., 2005; Verschueren et. al.,

2004). However, other studies have reported no effect of WBV on postural balance, especially when balance is tested in double leg stance (Bogaerts et. al., 2011; Marín et. al., 2011). In contrast, the effect of WBV on single leg standing balance showed a significant improvement following the WBV training, suggesting that single leg balance is more compromised in older adults (Jones et. al., 2013; Gusi et. al., 2006; Rees et. al., 2009). WBV therapy may be an alternative intervention for older adults who are unable to perform the conventional strengthening exercise due to limited mobility, functional performance and pain.

Segmental Vibration Therapy

In some cases, whole body vibration therapy has been shown to provide effective benefits without strenuous effort such as that required during aerobic

53 or resistance training. However, WBV is not directed to a specific muscle group and the stimuli is widespread unless dynamic movements of certain muscle groups are incorporated into the vibration protocol. In contrast, segmental vibration therapy (SVT) can be used to target specific muscle groups. The vibration can be directly targeted to a muscle group of interest and participants receiving vibration therapy can be in a seated position

(Ridgel et. al., 2013; Peer et. al., 2009). In addition, SVT minimizes side effects such as dizziness and nausea, which often result from stimulation of the whole body (Cronin et. al., 2004). Additionally, the stimulus is directly applied to the region of interest frequency can be lower than what is used for whole body vibration therapy and still show beneficial effects of improved ankle and hamstring flexibility and perceived stiffness (Peer et. al., 2009).

According to Paoloni and colleagues (2014), segmental muscle vibration can modulate muscle activity and induce a low degree of co- activation of antagonist muscles of the arm during a reaching movement. SVT has also been used to treat ankle sprains and hamstring injuries in healthy adults resulting in significant acute effects of improving flexibility and reducing perceived stiffness (Peer et. al., 2009). Additionally, SVT has been used as a therapy for post-stroke patients to improve motor function (Caliandro et. al.,

2012) and reduce spasticity of hemiplegic limbs (Noma et. al., 2009, 2012).

These effects of SVT on muscle activity provide a potential therapy for the age-related changes in muscle function, such as stiffness and flexibility, that affect postural balance in older adults.

The demonstrated link between balance, muscle function and vibration

54 therapy indicates the potential of a vibration therapy, specifically segmental vibration therapy (SVT), to improve balance through proprioceptive stimulation that promotes motor recruitment on muscle in the lower limbs.

Therefore, this study aims to determine the effectiveness of three sessions of

SVT to alter lower leg muscle activation and improve balance in healthy older adults. We hypothesize that the segmental vibration therapy: 1) will improve balance during a double leg stance in different conditions that challenge sensory inputs which play a role in maintaining balance and 2) will elicit improved motor recruitment during the balance task.

Methods

Subject population

Twenty individuals over 60 years old were recruited from the community for this study. Individuals with more than one sign or symptom of cardiovascular disease, pulmonary disease, and acute neurological impairment or on treatment that alters balance and posture were excluded from participation in the study. Oral and written explanation of the study was offered to the participants. A written informed consent was obtained according to the guidelines of the Kent State University Institutional Review Board (IRB) and each participant signed the consent before they started with the study.

Study Protocol

Participants came to the Motor Control Lab at Kent State University on 3 consecutive days for the study. The participants were randomized into either a

55 vibration therapy (SVT) or control (CON) group. On the first day, baseline measurements of the maximum voluntary contractions (MVCs) with electromyograms (EMGs), fall risk test and modified clinical test of sensory integration and balance (m-CTSIB) with EMG recordings were obtained.

Participants then received segmental muscle vibration therapy of the lower leg muscles at 20Hz for 2 minutes (SVT) or rest in a seated position with no vibration (CON). On the second day, participants came in only for the segmental vibration therapy or rested in a seated position with no vibration stimuli. On the third day, the participants received the segmental vibration therapy first followed by the post intervention assessments of the MVCs with

EMGs, fall risk test and m-CTSIB with EMG recordings.

Fall Risk and Balance Assessment

The Biodex Balance System (Biodex Medical Systems, Inc, Shirley, NY) was used for the fall risk test and the modified clinical test of sensory integration and balance (m-CTSIB) was used to assess sensory integration capabilities and balance. The fall risk test was performed as a baseline measurement and post intervention to obtain the overall stability index as the primary outcome measure. The overall stability index is the average displacement from the center of gravity in all motions in degrees while the subject is quietly standing when the platform is loosened. Overall stability index was averaged after three test trials of 20 seconds each. A higher score is indicative of larger postural sway during the test demonstrates instability and an increased risk of falls. The m-CTSIB test assesses balance with the contribution of three sensory systems that play a role in maintaining postural balance. Four

56 sensory conditions make up the m-CTSIB test. The first condition, eyes open on a firm surface (EOFS), allows the subject to use the visual, vestibular and somatosensory system to maintain their balance. In the second condition, eyes closed on a foam surface (ECFS), visual input is omitted and the subject depends on vestibular and somatosensory input. In the third condition, eyes open on a soft surface (EOSS), the somatosensory system is challenged, and the subject depends on visual and vestibular inputs. Lastly, in the fourth condition, eyes closed on a soft surface (ECSS), the subject solely depends on the vestibular system to maintain their postural balance. For each test condition, participants held a double leg stance for 20 seconds. For the soft surface, a foam pad was placed on the same position as the firm surface of the Biodex Balance system. In order to ensure safety of this older population, a safety harness was used to secure the participants and to prevent falling.

There was also a support bar available for them to grasp, if needed. Sway index scores were obtained after each 20 seconds balance test condition. The sway index is the average position of the subject from their center of balance

(Guskiewicz et. al., 1996) and a higher sway index score indicates instability and loss of balance.

Intervention: Segmental Vibration Therapy

The Swisswing (Swiss TTP, Twinsburg, OH) was used to administer the vibration stimuli. The soleus, gastrocnemius and tibialis anterior muscles were stimulated for 2 minutes at 20Hz for 3 sessions, one session per day for 3 consecutive days. The lower leg muscles, specifically the soleus and lateral gastrocnemius, was stimulated by direct placement of the subject’s lower leg

57 on the Swisswing while seated. The tibialis anterior was stimulated by the subject placing the lateral side of their lower leg against the Swisswing for stimulation. The control group sat and placed their lower leg on the Swisswing the same way as the control group, but the vibrations were not turned on.

Electromyograms

Electromyograms (EMG) recordings from the soleus, tibialis anterior and gastrocnemius was recorded on the self-selected dominant leg using surface electrodes (Noraxon USA Inc, Scottsdale, AZ). The participants’ skin surface was wiped with ethanol swabs and sand paper was used to gently abrade the skin for the electrodes to adhere. Bipolar surface electrodes were placed on the belly of the muscle (soleus, lateral gastrocnemius and tibialis anterior).

Additionally, tape was used to secure the electrodes if they fail to adhere to the skin surface. In order to normalize the EMG data, a maximum voluntary contraction (MVC) EMG was collected by having the individuals complete a modified dorsiflexion with maximum contraction of the soleus and tibialis anterior and a toe stand to facilitate a plantar flexion for maximum contraction of the gastrocnemius. Participants had a steady support to hold on to and verbal cues were given to make sure each subject performs the exercise correctly and safely. Baseline EMG data was collected during balance assessments of a double leg stance during the different conditions that challenged sensory inputs. The raw EMG signal was normalized by full-wave rectification, smoothed at 100ms root mean square (RMS) and bandpass filtered (between 10Hz and 1kHz). Mean amplitudes for muscle activation during the balance assessment were expressed as a percentage in relation to

58 the MVC obtained for each muscle. MVC and EMG data during balance assessment were repeated post vibration stimuli.

Statistical analysis

An independent sample t-test was used to compare the demographic variables (age, height, weight and gender) of the control and vibration therapy

(SVT) group. A repeated measure ANOVA (2 time X 2 groups) was used to determine the changes in overall stability index scores for fall risk between the control and the SVT group. A repeated measure ANOVA (2 groups x 2 time) was used to compare the sway index scores and the mean EMG amplitude for each of the four m-CTSIB conditions separately. A paired t-test was used to compare the pre-post means in each group, if there was a significant interaction or main effect of time or group. IBM SPSS Statistics 25 was used to run the analysis.

Results

Twenty participants were enrolled for the study and randomized into either

CON or SVT group. There were no significant differences in age, height and weight between the two groups (Table 1).

Table 1. Demographic characteristics of participants in both groups.

CON (n=10) SVT (n=10) p value Age 66.60 ± 5.32 68 ± 7.54 0.637 Females/Males (n) 7/3 5/5 - Height (m) 1.67 ± 0.77 1.72 ± 0.57 0.145 Weight (kg) 68.30 ± 9.46 71.93 ± 11.68 0.455

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Data represented as mean ± SD.

Fall Risk and Balance Assessment

There was no interaction between group and time in the fall risk stability index scores (F = 0.490, p = 0.493, stability index (mean ± std) CON pre:1.120 ± 0.25 post: 1.070 ± 0.58; SVT pre: 1.31 ± 0.66 post:1.18 ± 0.51). A paired t-test also showed that there was no main effect of time in either group, CON pre- post (t = 0.324, p = 0.753, Figure 1) and SVT pre-post (t = 1.197, p = 0.262, Figure 1).

Figure 1. Box plot represents data for fall risk pre-post CON vs SVT.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between groups (F = 0.490, p = 0.493). No observed main effect of time in each group, CON pre-post (t = 0.324, p = 0.753) and SVT pre-post (t = 1.197, p = 0.262).

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There was no significant interaction between the groups with the m-CTSIB scores in all four conditions (EOFS: F = 6.14, df = 1, p = 0.443, Figure 2a; ECFS: F = 0.079 , df = 1, p = 0.782, Figure 2b; EOSS: F =0.023 , df = 1 , p = 0.881, Figure 3a; ECSS: F = 0.034, df = 1 , p = 0.857, Figure 3b). A paired t- test comparing the mean pre-post sway index within each group also showed no significant difference. However, the SVT group in the EOSS condition showed a reduced mean post sway index of 20% that was approaching significance (t = 1.972, p = 0.080, Figure 3a).

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a

b

Figure 2. Box plot of m-CTSIB sway index scores CON vs SVT during the firm surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the m-CTSIB scores in the EOFS (a) and ECFS (b) conditions. No observed main effect of time for each group.

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a

b

Figure 3. Box plot of m-CTSIB sway index scores CON vs SVT during the soft surface conditions

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the m-CTSIB scores in the EOSS (a) and ECSS (b) conditions. No observed main effect of time for each group.

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Muscle Activity EMG MVCs and average amplitude (µV) for the soleus, lateral gastrocnemius and tibialis anterior were analysed for each m-CTSIB balance condition separately. The average amplitude was expressed as a percentage of the

MVC. No significant interactions were observed between the groups with all the muscles and in all four conditions. Soleus (EOFS: F = 0.687, df = 1, p =

0.418, Figure 4a; ECFS: F = 0.386, df = 1, p = 0.542, Figure 4b; EOSS: F

=0.083, df = 1, p = 0.777, Figure 5a; ECSS: F = 0.000, df = 1, p = 1.0, Figure

5b).

Lateral Gastrocnemius (EOFS: F = 2.784, df = 1, p = 0.113, Figure 6a;

ECFS: F = 2.785, df = 1, p = 0.112, Figure 6b; EOSS: F = 2.642, df = 1, p =

0.122, Figure 7a; ECSS: F = 0.461, df = 1, p = 0.506, Figure 7b).

Tibialis anterior (EOFS: F = 0.024, df = 1, p = 0.878, Figure 8a; ECFS:

F = 0.764, df = 1, p = 0.394, Figure 8b; EOSS: F =0.730, df = 1, p = 0.404,

Figure 9a; ECSS: F = 0.004, df = 1, p = 0.950, Figure 9b).

The SVT group showed a significant decrease by 59% in the muscle activity of the tibialis anterior in the ECSS balance condition (t = 2.674, df = 9, p =

0.025, Figure 9b). The SVT group also showed an approaching significant decrease in post muscle activity of the lateral gastrocnemius in the EOSS by

45% (t = 1.923, df = 9, p = 0.087, Figure 7a), ECSS by 56% (t = 2.231, df = 9, p = 0.053, Figure 7b) and of the tibialis anterior in the ECFS by 51% (t =

2.042, df = 9, p = 0.072, Figure 8b).

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a

b

Figure 4. Box-plots of soleus muscle activity CON vs SVT during the firm surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the muscle activity in the EOFS (a) and ECFS (b) conditions. No observed main effect of time for each group.

65

a

b

Figure 5. Box-plots of soleus muscle activity CON vs SVT during the soft surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the muscle activity in the EOSS (a) ECSS (b) conditions. No observed main effect of time for each group.

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a

b

Figure 6. Box-plot of lateral gastrocnemius muscle activity CON vs SVT during firm surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the muscle activity in the EOFS (a) and ECFS (b) conditions. No observed main effect of time for each group.

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a

b

Figure 7. Box-plot of lateral gastrocnemius muscle activity CON vs SVT during soft surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the muscle activity in the EOSS (a) and ECSS (b) conditions. No observed main effect of time for each group.

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a

b

Figure 8. Box-plot of tibialis anterior muscle activity CON vs SVT during firm surface conditions

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the m-CTSIB scores in all the EOFS (a) and ECFS (b) conditions.

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a

b

Figure 9. Box-plot of tibialis anterior muscle activity CON vs SVT during soft surface conditions

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the m-CTSIB scores in all four conditions. The SVT group showed an interaction of time in the muscle activity of the tibialis anterior in the ECSS balance condition (p = 0.025; t = 2.674) (Figure 9.d).

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Discussion

The objective of this study was to determine the effect of 3 sessions of SVT on postural balance and muscle activity in older adults. Our results did not indicate an overall significant difference between the CON and SVT groups.

However, the vibration therapy had some observed effect in the muscle activity of SVT group during the balance conditions with only 2 of the 3 sensory inputs. There was also an approaching significant decrease in the m-

CTSIB scores of the SVT group in the EOSS balance condition.

Various age-related changes in postural control systems have been observed in older adults over 65 years old who have reported falls (MacRae et. al.,

1992). The postural balance dysfunction can result from sensory and motor impairments caused by pathology or loss of function due to normal ageing. A decline in proprioception, specifically of the lower limbs, has a strong association with balance deficits in the elderly (Woollacott et. al., 1986 and

Manchester et. al., 1989). Within the peripheral nervous system (PNS), mechanoreceptors undergo anatomical and physiological changes due to ageing (Shaffer & Harrison, 2007). Spindle fibers change in function caused by decreased sensitivity and increased capsular thickness (Miwa et.al., 1995).

Denervation due to muscle atrophy and deterioration of spinal presynaptic inhibition pathways also play a role in the loss of function (Swash & Fox, 1972 and Burke et. al., 1996). The number of golgi tendon organs are also significantly reduced with ageing (Aydog et. al., 2006).

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Vibration therapy stimulates muscle spindles of the somatosensory system which activate alpha-motor neurons to generate muscle contraction through a spinal reflex mechanism (Cardinale and Bosco, 2003; Gribble et. al., 2004; Cochrane et.al., 2011). In older adults this can promote their function and improve sensitivity that can help improve their balance in challenging proprioceptive balance conditions as observed in our data where

SVT reduced the m-CTSIB sway index scores of the SVT group in the EOSS balance condition.

With increasing age, there is a decrease in muscle strength of the legs and core muscles (Shumway-Cook & Woollacott, 2001). This leads to a compensatory mechanism of increased activation of the ankle muscle that play a key role in ankle stability, the soleus and gastrocnemius and increased co-activation of agonist muscles, the tibialis anterior, which would normally not occur in a healthy, younger individual (Macaluso & De Vito, 2004 and Shaffer

& Harrison, 2007 and Nagai et. al., 2012). This compensatory co-activation is further increased when visual input is reduced or not available, resulting in an increased dependence on the ankle strategy for stabilizing postural balance.

The observed decrease in muscle activity of the gastrocnemius in the

EOSS and ECSS condition, and tibialis anterior in the ECFS and ECSS condition in the SVT group in this study indicates that SVT modulated the compensatory increased muscle activation that is usually observed in older adults. Furthermore, for this study, participants had direct placement of their calf and the lateral side of the lower leg against the Swisswing for stimulation.

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The observed effect of decreased muscle activity of the gastrocnemius and tibialis anterior but not the soleus suggests that directly targeting the vibration stimuli to the muscle of interest will have a better outcome of getting an effect.

Although our results may not have elicited significant effects of SVT on balance in older adults, the small effects do support the theory of vibration therapy being a possible low risk intervention for balance in older adults.

However, there has been conflicting results on vibration therapy outcomes and balance the various protocols used. Long-term training has shown improvements or no effect, but single sessions or shorter training times did have a positive effect on balance. A single session of WBV therapy improved single leg balance but had no effect on joint leg position and mobility in older adults (Jones et. al., 2013). Torvinen and colleagues (2002) also observed an improvement in postural sway following only 4 minutes of WBV training in younger adults. Furthermore, there has been extensive variability in the vibration frequencies and vibration devices used among these different studies. Lam et. al., (2012) WBV analysis showed that a vibration frequency range of 35-40Hz had no effect on balance while a range between 12.6Hz to

26Hz had significant results with the balance, mobility and falls in older adults.

For this study, we used a vibration frequency of 20Hz over 3 sessions over 3 consecutive days and only measured the outcome at baseline and post vibration on the third day.

This study had several limitations that could have influence the outcome of our results. First, there was a wide variability in the muscle activity among all

73 the participants. This variability affected the magnitude of effect of the vibration intervention which did not result in a statistically significant outcome.

Secondly, our study design of 3 SVT session, one session per day for 3 consecutive days and only recording baseline and outcome measurements on the first and third day respectively, did not allow us to determine whether there was a gradual effect over time from the first session of SVT. In hindsight, it would have been helpful to collect EMG measurements on each day after the vibration stimuli which would have given us an opportunity to assess the effects of SVT over the 3 consecutive days. Lastly, we only evaluated the effects of the SVT on the third day and did not have any follow up assessments. Therefore, our study did not assess whether the observed effects were temporary or if they lasted longer than immediately post vibration stimulus.

Conclusion

Our present study did not provide a significant effect that SVT improves fall risk and balance in older adults. It also did not show a significant effect in lower muscle activity during the different balance conditions. However, there was an observed decrease in muscle activity of the SVT group in the more challenging balance conditions that does suggest that further research should be conducted to give a clear effect of SVT. This study also adds the conflicting results of vibration therapy on balance in older adults because of the different protocol and vibration frequency used, even though it was still in the range of previously suggested effective frequencies. The use of SVT

74 instead a WBV did provide better targeting of the focus area and less adverse effects but more research needs to be done with study design that focuses on the repeated use of SVT over a longer period and with a study population that would have less variability in their baseline measurements.

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III. THE EFFECT OF SEGMENTAL VIBRATION THERAPY ON EXECUTIVE FUNCTION.

Introduction

Cognitive decline and falls in the elderly were previously seen as unrelated geriatric conditions. However, several studies have documented a correlation between cognitive impairment and falls (Liu-Ambrose et. al., 2008; Gleason et.al., 2009; Mirelman et. al., 2012), even in the absence of dementia (which dramatically increases the risk of falls, Tinnet, 2003; Holtzer et. al., 2007;

Hermal et. al., 2010). Cognitive processes such as executive function and attention are required to maintain balance during gait and standing (Smith-

Ray et. al., 2013). Executive function is a set of cognitive skills needed to complete a series of goal directed complex actions which require planning and monitoring (Lezak et.al., 2004). Low performance scores in specific cognitive domains of executive function namely, attention, memory and visuospatial function have been associated with increased risk of falls in individuals who are cognitively impaired and cognitively unimpaired (van

Schoor et. al., 2002; Tinnet, 2003; Holtzer et. al., 2007; Herman et. al., 2010;

Martin et. al., 2009).

With increasing age, executive function and attention decline while motor tasks such as balance and walking become less automated and more cognitively taxing (Schaefer and Schumacher, 2011). Studies have shown

83 that cognitive training, as well as motor cognitive dual-task training, improves gait and balance in young and older adults (Li et. al., 2010; Smith-Ray et. al.,

2013; Lindenberg et. al., 2000). The interventions and cognitive training improved cognitive functions and subsequently balance by influencing visuospatial working memory, processing speed and inhibition (Smith-Ray et. al., 2013).

An alternative intervention that has shown promising beneficial effects with no strenuous effort, easy administration and less risk of injury is vibration therapy. Whole body vibration (WBV) has shown to promote beneficial physiological effects such as increase in oxygen-uptake, blood flow, intra- muscular temperature and improved muscle power (Rittweger et. al., 2002;

Cochrane et. al., 2008; Herrero et. al., 2011). These improvements, specifically oxygen uptake and blood flow could improve cognitive function. In addition, animal studies have documented improved maze learning and enhanced neuronal activity in mice following whole body vibration (Keijser et. al., 2011) and WBV training improved inhibitory control in adults with attention deficit hyperactivity disorder (ADHD) and healthy children (Fuermaier et. al.,

2014; den Heijer et. al., 2015). The possible effect of WBV on cognitive domains is from the stimulation of mechanoreceptors which have neuroanatomical connections to cognitive brain areas in the pre-frontal cortex

(Kolb and Whishaw, 2009; Regterschot et. al., 2014)

However, WBV has also been associated with side effects such as dizziness, nausea and disorientation (Cronin et. al., 2004; Slota et.al., 2008).

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Segmental vibration therapy (SVT), which is vibration therapy targeting a specific muscle group, may provide similar beneficial effects on cognition without the limitations of WBV. The purpose of this study was to determine whether the SVT improves executive function specifically, the speed of processing, visuospatial working memory and attention/inhibitory control in older adults. The hypothesis is that three sessions of segmental vibration therapy will improve executive function in healthy older adults.

Methods

Subject population

Twenty individuals over 60 years old were recruited from the community for this study. Individuals with more than one sign or symptom of cardiovascular disease, pulmonary disease, and acute neurological impairment or on treatment that alters balance and posture were excluded from participation in the study. Oral and written explanation of the study was offered to the participants. A written informed consent was obtained according to the guidelines of the Kent State University Institutional Review Board (IRB) and each participant signed the consent before they started with the study.

Study Protocol

Participants came in for the study on 3 consecutive days. The participants were randomized into either a segmental vibration therapy (SVT) or a control group (CON). On the first day, baseline measurements of executive function using the National Institute of Health (NIH) Toolbox were obtained.

Participants then received either segmental muscle vibration therapy of the

85 lower leg muscles at 20Hz for 2 minutes (SVT) or rested in a seated position with no vibration (CON). On the second day, participants came in for another session of SVT or rest in a seated position. On the third day, the participants completed the final SVT session or rest followed by post intervention assessments of executive function.

Intervention: Segmental Vibration Therapy

The Swisswing (Swiss TTP, Twinsburg, OH) was used to administer the vibration stimuli. The soleus, gastrocnemius and tibialis anterior muscles were stimulated for 2 minutes for each muscle group at 20Hz for 3 sessions, one session per day for 3 consecutive days. The soleus and lateral gastrocnemius were both stimulated by direct placement of these muscles on the Swisswing while seated. The tibialis anterior was stimulated by placing the lateral side of their lower leg against the Swissswing. The CON group sat and placed their lower leg on the Swisswing similar to the SVT group, but the vibration was not turned on.

Executive function tests

Participants completed executive function tests in the NIH toolbox on an iPad.

Three separate tests were used to assess inhibitory control and attention, working memory and processing speed. The Flanker inhibitory control and attention test assessed the participant’s ability to focus on a given stimulus while inhibiting attention to another stimulus. The stimulus in this test is a row of 5 arrows pointing in different directions and participants must focus on the

86 direction of the middle arrow. Scoring of the Flanker Inhibitory control and attention test was based on accuracy and reaction time with a computed score between 0 - 10. If the participant’s accuracy was less than or equal to

80%, the computed final score will only include the accuracy score. If the participants accuracy was greater than 80%, the accuracy and reaction time scores are combined to give the computed score. The fully corrected T-score is corrected for age, gender, education and ethnicity using the NIH toolbox national represented normative sample with a mean of 50 and a SD of 10.

The list sorting working memory test assesses the ability of immediate recall and sequencing of different visually and orally presented stimuli. Different animals and foods are displayed with accompanying audio and text. The participant is asked to say the presented list of items in size order from smallest to largest. The first part of the test is single-dimensional, the list is either food or animals. The second part of the test is two-dimensional, the list includes both food and animals and the participant must try to recall and say the food first from smallest to largest, followed by the animals. To evaluate simple changes over time the raw scores were used for analysis. The raw score is calculated by summing the number of items correctly recalled and sequenced in the single and two-dimension lists and scores range from 0 –

26.

Lastly, the pattern comparison processing speed test measures the participant’s speed of processing information by asking them to determine whether two side by side pictures are the same or not. Participants are given

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90 seconds to respond to as many as possible and they can get up to a maximum of 130 images (NIH, 2017). For simple changes over time, the raw score is used for analysis and it indicates the number of items answered correctly within 90 seconds and has a range of 0 – 130.

Statistical analysis

A repeated measure ANOVA 2 time (pre, post) X 2 groups (SVT, CON) was used to examine the changes in executive function for the three tests on attention and inhibition, working memory and processing speed. If there were significant differences in the repeated measures ANOVA, then paired samples t-test were used to assess which measures differed from each other. IBM

SPSS Statistics 25 was used to run the analysis.

Result

Twenty participants were enrolled in the study and were randomized into either CON or SVT group. Due to technical difficulties, only 14 of the participants data was reported for final analysis. There were no significant differences between age, height and weight between the two groups (Table

2).

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Table 2. Demographic characteristics of participants in both groups.

CON group (n=8) SVT group (n=5) p value

Age 66.75 ± 5.92 64 ± 1.1 0.288

Females/Males (n) 5/3 3/3 -

Height (m) 1.68 ± 0.08 1.74 ± 0.05 0.151

Weight (kg) 67.4 ± 10.47 76.04 ± 10.26 0.150

Data represented as mean ± SD.

Inhibition Control and Attention

No observed interaction between the groups was observed with the computed scores (F= 4.35, df = 1, p = 0.061, Figure 10). The fully corrected T-scores also showed no significant interaction between the groups (F = 2.35, df = 1, p

= 0.367, Figure 11).

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Figure 10. Box plot represents data for attention and inhibition computed scores.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between groups (F= 4.35, df = 1, p = 0.061).

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Figure 11. Box plot represents data for attention and inhibition fully corrected T- scores

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between groups (F = 2.35, df = 1, p = 0.367).

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Working Memory

A repeated measures ANOVA showed a significant interaction between the

groups in the raw scores (F = 5.31, df = 1, p = 0.042, Figure 8). The CON

group showed a slight increase in the mean score by 13%, but the SVT group

had a slight decrease by 4% in the mean scores (Figure 12). The fully

corrected T-score also showed a significant interaction between the groups

with a similar pattern of an increase by 13% in the CON group and a decrease

by 7% in the SVT group (F = 5.526, df = 1, p = 0.041, Figure 13).

Figure 12. Box plot represents data for working memory raw scores.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. Interaction observed between the groups (F = 5.31, df = 1, p = 0.042).

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Figure 13. Box plot represents data for working memory fully corrected

T- scores.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. Interaction observed between groups (F = 5.526, df = 1, p = 0.041).

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3. Processing Speed

A repeated measures ANOVA showed a significant interaction between the

groups in the mean raw scores (F = 5.47, df = 1, p = 0.039, Figure 14). The

CON group had an increase in mean raw scores by 18% and the SVT group

increase by 12%. The fully corrected T-score did not show significant

interaction between the groups (F = 3.978, df = 1, p = 0.074, Figure 15). Even

though both the CON and SVT groups had increased performance post

intervention of 22% and 21% respectively.

Figure 14. Box plot represents data for processing speed raw scores.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. Interaction observed between groups (F = 5.47, df = 1, p = 0.039).

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Figure 15. Box plot represents data for processing speed fully corrected T-scores.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction observed between groups. No observed main effect of time.

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Discussion

The executive function measures of this study are considered fluid-ability measures, which improves from childhood and adolescence, then declines in adulthood and gets further impaired in old age (NIH, 2012). This old age impairment has been correlated with an increase in falls and balance impairment in the elderly even in the absence of cognitive disorders (Hermal et. Al., 2010; Mirelman et. Al., 2012). The SVT resulted in an acute improvement in processing speed as measured by the Pattern Comparison

Processing Speed test. We hypothesized that the SVT would improve executive function in older adults by stimulation mechanoreceptors that have neuroanatomical connections to cognitive brain areas in the pre-frontal cortex

(Braak et. Al., 1996; Kolb and Whishaw, 2009; Regterschot et. al., 2014)

WBV stimulates muscle spindles, as well as mechanoreceptors in the skin, which send afferent signals to the primary somatic sensory cortex

(Martin, 2003). The sensory cortex has direct and indirect connection to the prefrontal cortex, which plays a key role in cognitive function (Braak et. al.,

1996; Smith and Jonides, 1999; Kolb and Whishaw, 2009). Furthermore, the limbic system, which is important for learning and memory, provides an indirect pathway between the sensory region and the prefrontal area (Braak et. al., 1996). Therefore, the sensory stimulation from the SVT could influence neural activity in the sensory cortex as well as brain regions linked to the sensory cortex that play a role in cognitive function.

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The Flanker Inhibitory Control and Attention Test assessed the participants ability to handle an abundance of environmental stimulation which can be crucial during gait and daily balance tasks. Vibration therapy, specifically, whole body vibration (WBV) has shown to have acute beneficial results in inhibitory control as a measure of attention in healthy adults and those with ADHD using the Stroop Colour Word Interference task (Fuermaier et. Al., 2014). Our results did not show a significant difference between the groups post intervention measures. However, the small sample of healthy older adults produced a p value of 0.061 and a power analysis using the means of the two groups indicated an effect size d = 1.06 was present and the

SVT effects on inhibitory control and attention would have been significant with a larger sample size of 24 participants with 12 in each group.

Few studies have examined the effect of vibration therapy on inhibition control and attention but there has been an established correlation between cognitive tasks and postural task. Hausdorff and colleagues (2005) observed that older adults who performed well on a Stroop test had better walking performance as measured with stride time variability. Similar correlation results were observed when the relationship between cognitive function and falls in the elderly (Holtzer et al. 2007). Our results did not show any correlation between fall risk and the executive function measures in either group pre and post intervention. Furthermore, unlike the acute beneficial effects of WBV on attention and inhibition in healthy adults with ADHD

(Fuermaier et. Al., 2014), our study only did vibration therapy on the lower

97 legs over 3 days, so its beneficial effects could be acute and may only manifest directly after the vibration stimuli.

We looked at the three domains of executive function because of the role they play during balance and gait. The Flanker Inhibitory Control and Attention test focuses on selective attention because it requires the focus and processing of a central object while inhibiting the other elements that can be distracting

(Borel and Alescio -Lautier, 2013).

The processing speed test measured the participant’s mental efficiency, which is the amount of information that the subject can process within a given time and the working memory test measured the ability of the participant to store, process information over a series of task during a brief period of time (NIH,

2017). These three domains are collectively necessary for decision making, which can be crucial during gait and associated perturbations to allow postural corrections and foot placement to maintain postural balance.

We had several observed limitations in this study. The small sample size as mentioned earlier, limited the significant effect of the SVT intervention for this part of the study. A higher sample size with equal numbers in each group would have provided a better insight into the effects of the SVT intervention between the groups. The study design we used for this study was 3 sessions of SVT, one session per day at the same time for 3 consecutive days. We only collected baseline measurements and post intervention measurements on the third day. Previous studies on the effect of vibration therapy have observed an effect immediately after the vibration intervention. Our study

98 design prevented us from observing the immediate effect of SVT and if there would have been a gradual effect over the three days. Our collected data could only indicate the effects of SVT for that last day when post intervention measurements were collected.

Conclusion

In this study we hypothesized that SVT will improve processing speed, working memory and inhibition control and attention in healthy adults over 60 after receiving 3 sessions of SVT. Our results indicated that processing speed and inhibitory control and attention improved following SVT but working memory did show changes between the groups. Furthermore, our data did not indicate a correlation between executive function scores and fall risk in our study population. Further studies need to be conducted to examine the effect of vibration therapy on executive function. There is extensive variability in the study designs, vibration therapy application and outcome measures, which makes it hard to compare these results. However, since there is some observed effect, studies focusing on the mechanisms of those effects would provide better insight into the use of vibration therapy as an intervention for cognitive functions. Executive function is essential for postural control during different postural tasks, and with the observed correlation between cognitive function and postural control it is of importance to continue to examine the role of cognitive health on postural performance and balance in older adults.

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IV. THE EFFECT OF SEGMENTAL VIBRATION THERAPY ON DUAL TASKING POSTURAL BALANCE IN OLDER ADULTS.

Introduction

Postural balance and dual-tasking

Postural balance during upright quiet stance requires the integration of sensory inputs from the visual, vestibular and somatosensory system as well as the motor system which provides output for the muscle tone required to maintain posture. Additionally, cognitive processing is required to integrate motor and sensory feedback during daily balance tasks.

The role of cognitive processes during balancing tasks is usually unconscious during daily tasks. However, there are several situations when postural balance occurs during a cognitive task: walking while talking or a simple task of standing while thinking. The task of maintaining postural balance while performing a cognitive task is termed dual-tasking postural control (Huxhold et.al., 2006). Cognitive processing during balance tasks is mostly identified during balance tasks with anticipated perturbations that require postural adjustments (Massion, 1992; Wollacott and Shumway-Cook, 2000). This unconscious dual-tasking postural control occurs to integrate multi-sensory feedbacks which assist in monitoring and maintaining postural balance

(Wollacott and Shumway-Cook, 2000).

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During dual tasking postural control when a mental task is performed, there is a conscious requirement of attention to both the balancing and mental task at hand. This causes a competition for attention resources and the attention capacity is tested. When attention is required for two separate tasks, the availability of attention resources is limited and performance of either task will not be completed effectively (Huxhold et. al., 2006; Borel and Alescio-Lautier,

2014). This is particularly observed in situations when balancing during conflicting sensory conditions while performing a mental task that requires a response (Yardley et. Al., 2001; Dault et. al., 2003).

Ageing and dual-tasking

Increase in age brings an increased risk of falls. Age-related changes in the sensorimotor system leads to a deterioration in postural balance thus increases the risk of falls (Horak et. al., 1989; Wollacott, 2000; Lacour et. al.,

2008). The decline in balance control as a result of age-related cognitive impairments has been an area of interest in understanding posture – dual tasking interactions. Older adults have shown to have increased instability during dual-tasking postural balance that requires attentional demands on two tasks (Shumway-Cook and Wollacott, 2000; Weeks et. al., 2003; Wollacott and Shumway-Cook, 2002).

The decline in dual-task postural balance in older adults could be the results of reduced processing speed and/or deficits in the allocation of attention resources (Andres and van der Linden, 2000; Brauer et. al., 2001).

Additionally, there has been an observes increase in attention during simple

105 postural control tasks in older adults (Wollacott and Shumway-Cook, 2002; Li et. al., 2005). Therefore, the added attentional demand of a cognitive task would increase the overall attentional demands and push older adults to their attention capacity and reduce effectiveness of either task making them susceptible to falls (Borel and Alescio-Lautier, 2014).

Training interventions to improve dual-tasking

Cognitive training interventions that focus on attention and working memory have been used to improve cognitive function in older adults. Various training programs have used working memory and attention tasks in the training programs and have observed improvements in that task and other untrained executive function domains. Borella et. al., 2010 showed that a working memory training program improved working memory in older adults as well as untrained domains such as attention and processing speed. Similarly, Li et. al., 2008 and Buschkuehl et. al., 2008 also indicated a transfer of improvement in other domains following a working memory training program.

This improvement in executive function can contribute to improved postural balance during dual tasking postural balance.

Other studies have focused of dual- task training to improve the allocation of attentional resources between multiple tasks. Li et. al., 2010 showed that a dual task training on visual and auditory tasks improved attention control in young and older adults as well as reduced postural sway while standing on a stable platform. A dual-task training program of attention and a working

106 memory task showed a beneficial effect on the executive domains trained as well as improved performance in a postural task (Borel et. al., 2012). Borel and colleagues (2013) have suggested that the improvement of executive functions through cognitive training has a positive effect on the processing of sensory information which can improve the sensory integration required in postural balance.

Other dual- task interventions to improve dual task postural control in older adults have focused on a physical intervention with a concurrent cognitive task to improve dual task postural control. Pichierri et. al., 2012 showed that older adults who took part in a cognitive-motor exercise intervention had an improvement in dual-tasking voluntary step execution.

Physical activity such as aerobic and strength training has shown to be a protection for cognitive decline (Northey et. al., 2018; Norton et.al., 2014) and to improve brain function and connectivity (Voelcker-Rehage et. al., 2011;

Voss et. al., 2010). This effect can mediate the decline in dual tasking by improving efficiency in mental tasks as well as strengthening muscle groups used during postural balance. However, performing a physical exercise for older adults can cause a lot of strain and increased risk of injury. Whole body vibration (WBV) has been studied as an alternative to physical activity due to its low risk of falls and injury in older adults. The vibration therapy stimulates muscles spindles to initiate a muscle contraction (Bogaerts et al., 2007).

Several studies have shown that WBV has improved muscle performance and postural balance (Bruyere et. al., 2005; Bogaerts et. al., 2011; Pollock et. al.,

2012). The use of vibration therapy has shown potential to be an alternative

107 intervention for older adults, therefore using segmental vibration therapy would produce similar or better improvements by directing the vibration therapy to specific areas of interest without the adverse effects (dizziness and nausea) of WBV (Cronin et. al., 2004). Our hypothesis is that SVT will improve dual- task postural balance in older adults. We will administer 3 sessions of SVT and measure balance assessments while participants perform a serial subtraction as the secondary task.

Methods

Subject population

Twenty individuals over 60 years old were recruited from the community for this study. Individuals with more than one sign or symptom of cardiovascular disease, pulmonary disease, and acute neurological impairment or on treatment that alters balance and posture were excluded from participation in the study. Oral and written explanation of the study was offered to the participants. A written informed consent was obtained according to the guidelines of the Kent State University Institutional Review Board (IRB) and each participant signed the consent before they started with the study.

Study Protocol

Participants came to the Motor Control Lab at Kent State University for the study on 3 consecutive days. The participants were randomized into either a vibration therapy (SVT) or control (CON) group. On the first day, baseline measurements of the maximum voluntary contractions (MVCs) with electromyograms (EMGs) and dual tasking modified clinical test of sensory

108 integration and balance (m-CTSIB) with EMG recordings were obtained.

Participants then received segmental muscle vibration therapy of the lower leg muscles at 20Hz for 2 minutes (SVT) or rest in a seated position with no vibration (CON). On the second day, participants came in only for the segmental vibration therapy or rested in a seated position with no vibration stimuli. On the third day, the participants received the segmental vibration therapy first followed by the post intervention assessments of the MVCs with

EMGs, dual tasking m-CTSIB with EMG recordings.

Intervention: Segmental Vibration Therapy

The Swisswing (Swiss TTP, Twinsburg, OH) was used to administer the vibration stimuli. The soleus, gastrocnemius and tibialis anterior muscles were stimulated for 2 minutes at 20Hz for 3 sessions, one session per day for 3 consecutive days. The lower leg muscles, specifically the soleus and lateral gastrocnemius, was stimulated by direct placement of the subject’s lower leg on the Swisswing while seated. The tibialis anterior was stimulated by the subject placing the lateral side of their lower leg against the Swisswing for stimulation. The control group sat and placed their lower leg on the Swisswing the same way as the control group, but the vibrations were not turned on

Dual tasking

Participants performed a single task (cognitive task) and a dual task (balance and cognitive task) before and after the segmental vibration therapy. For the single task, participants performed a serial subtraction by 3 starting from a given number while in a seated position for 20 seconds (de Souza Fortaleza et. al., 2017). The Biodex Balance System (Biodex Medical Systems, Inc,

Shirley, NY) and the modified clinical test of sensory integration and balance

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(m-CTSIB) were used to assess sensory integration capabilities and balance during a simple thinking cognitive task for the dual tasking. Participants held a double leg stance for 20 seconds in four conditions: eyes open on a firm surface (EOFS), eyes closed on a firm surface (ECFS), eyes open on a soft surface (EOSS) and eyes closed on a soft surface (ECSS). During each m-

CTSIB test condition, participants were instructed to perform a simple cognitive task of serial subtraction by 3’s starting at a randomly assigned number (de Souza Fortaleza et. al., 2017). The serial subtraction by 3’s was started at different numbers for every test condition and session to prevent a learning effect. Correct and incorrect responses were recorded for the single task (ST) and dual task (DT) and were used to calculate the dual task cost for the motor and cognitive performance.

The dual task cost was used to quantify the subjects’ ability to perform a balance and a cognitive task concurrently and were calculated as follows:

Dual task cost in motor performance = 100*(DT motor measure – ST motor measure)/ST motor measure. The sway index scores were used as the motor measure and the ST motor measure was recorded from the balance test in previous sessions. Dual task cost in cognitive performance = 100*(DT correct answers – ST correct answers)/ ST correct answers (de Souza Fortaleza et. al., 2017). The dual task cost was calculated for each of the four m-CTSIB test conditions.

Electromyograms

Electromyograms (EMG) recordings from the soleus, tibialis anterior and gastrocnemius was recorded on the self-selected dominant leg using surface

110 electrodes (Noraxon, Scottsdale, Arizona). The participants’ skin surface was wiped with ethanol swabs and bipolar surface electrodes were placed on the belly of the muscle (soleus, lateral gastrocnemius and tibialis anterior). Sand paper was used to gently abrade the skin for the electrodes to adhere.

Additionally, tape was used to secure the electrodes if they fail to adhere to the skin surface. In order to normalize the EMG data, a maximum voluntary contraction (MVC) EMG was collected by having the individuals complete a modified dorsiflexion with maximum contraction of the soleus and tibialis anterior and a toe stand to facilitate a plantar flexion for maximum contraction of the gastrocnemius. Participants had a steady support to hold on to and verbal cues were given to make sure each subject performs the exercise correctly and safely. Baseline EMG data was collected during balance assessments of a double leg stance during the different conditions that challenged sensory inputs. The raw EMG signal was normalized by full-wave rectification, smoothed at 100ms root mean square (RMS) and bandpass filtered (between 10Hz and 1kHz). Mean amplitudes for muscle activation during the balance assessment were expressed as a percentage in relation to the MVC obtained for each muscle. MVC and EMG data during balance assessment were repeated post vibration stimuli.

Statistical analysis

An independent sample t-test was used to compare the demographic variables (age, height, weight and gender) of the control and vibration therapy

(SVT) group. A repeated measure ANOVA (2 groups x 2 time) was used to compare the sway index scores and the mean EMG amplitude for each of the four dual-tasking m-CTSIB conditions separately. A paired t-test was used to

111 compare the pre-post means in each group. IBM SPSS Statistics 25 was used to run the analysis.

Results

Twenty participants were enrolled for the study and randomized into either

CON or SVT group. An independent sample t-test was used to compare the age, gender, height and weight between the two groups, and none were significantly different (Table 3).

Table 3. Demographic characteristics of participants in both groups.

CON (n=10) SVT (n=10) p value Age 66.60 ± 5.32 68 ± 7.54 0.637 Females/Males (n) 7/3 5/5 - Height (m) 1.67 ± 0.77 1.72 ± 0.57 0.145 Weight (kg) 68.30 ± 9.46 71.93 ± 11.68 0.455 Data represented as mean ± SD.

Dual-task Balance Assessment

There was no significant interaction between the groups with the dual-tasking m-CTSIB scores in all four conditions (EOFS: F = 0.266, df = 1, p = 0.612,

Figure 16a; ECFS: F = 0.527, df = 1, p = 0.477, Figure 16b; EOSS: F = 0.630, df = 1 , p = 0.438, Figure 17a; ECSS: F = 0.001, df = 1 , p = 0.975, Figure

17b).

The CON group showed a decrease in mean sway index scores post intervention whereas the SVT had an increase in mean sway index scores in all conditions (Appendix C.1). A paired t-test comparing the mean pre-post

112 sway index within each group showed significant difference in the pre-post means of the CON group int the EOFS condition (t = 2.441, df = 9, p = 0.037,

Figure 16a).

113

a

b

Figure 16. Dual-tasking m-CTSIB sway index scores CON vs SVT during firm surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the m-CTSIB scores in the EOFS (a) and ECFS (b) condition. No observed main effect of time.

114

a

b

Figure 17. Dual-tasking m-CTSIB sway index scores CON vs SVT during soft surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the m-CTSIB scores in the EOSS (a) and ECFS (b) condition. No observed main effect of time.

115

Single-task vs dual-task balance assessment

There was no significant interaction between the groups with the single tasking vs. dual-tasking m-CTSIB scores in all four conditions (EOFS: F =

0.719, df = 1, p = 0.408, Figure 18a; ECFS: F = 0.442, df = 1, p = 0.515,

Figure 18b; EOSS: F = 0.109, df = 1 , p = 0.745, Figure 19a; ECSS: F =

0.131, df = 1 , p = 0.722, Figure 19b).

The CON had negative change scores in all DT balance conditions except for the ECFS condition. The SVT group had a negative change score in all ST balance conditions and in the DT ECFS balance condition (Appendix C. 2).

116

a

b

Figure 18. Single-task vs dual-tasking m-CTSIB sway index scores CON vs SVT during firm surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction observed between groups in the EOFS (a) and ECFS (b) conditions. No observed main effect of time.

117

a

b

Figure 19. Single-task vs dual-tasking m-CTSIB sway index scores CON vs SVT during soft surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction observed between groups in the EOFS (a) and ECFS (b) conditions. No observed main effect of time.

118

Muscle Activity

EMG MVCs and average amplitude (µV) for the soleus, lateral gastrocnemius and tibialis anterior were analyzed for each dual-tasking m-CTSIB balance condition separately. The average amplitude was expressed as a percentage of the MVC. No significant interactions were observed between the groups with all the muscles and in all four dual-tasking conditions. Soleus (EOFS: F =

0.349, df = 1, p = 0.562, Figure 20a; ECFS: F = 0.646, df = 1, p = 0.432,

Figure 20b; EOSS: F =0.001, df = 1, p = 0.974, Figure 21a; ECSS: F = 0.030, df = 1, p = 0.865, Figure 21b).

Lateral Gastrocnemius (EOFS: F = 2.143, df = 1, p = 0.160, Figure

22a; ECFS: F = 1.251, df = 1, p = 0.278, Figure 22b; EOSS: F = 2.155, df = 1, p = 0.159, Figure 23a; ECSS: F = 1.202, df = 1, p = 0.287, Figure 23b).

Tibialis anterior (EOFS: F = 0.924, df = 1, p = 0.349, Figure 24a; ECFS:

F = 1.354, df = 1, p = 0.260, Figure 24b; EOSS: F = 2.832, df = 1, p = 0.110,

Figure 25a; ECSS: F = 2.221, df = 1, p = 0.153, Figure 25b).

The CON group showed an approaching significant decrease in post mean muscle activity of the lateral gastrocnemius in the EOFS (p = 0.086; t = 1.929,

↓ 21%, Figure 22a), ECSS (p = 0.082; t = 1.954, ↓ 20%, Figure 23b). The SVT group showed an approaching significant increase in the post mean muscle activity of the tibialis anterior in the ECSS balance condition (p = 0.073; t = -

2.030, ↑ 23%, Figure 25b).

119

a

b

Figure 20. Box-plots of the dual-tasking soleus muscle activity CON vs SVT during firm surface conditions

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction observed between groups. No observed main effect of time.

120

a

b

Figure 21. Box-plots of the dual-tasking soleus muscle activity CON vs SVT during soft surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction observed between groups in the EOSS (a) and ECSS (b) conditions. No observed main effect of time for each group.

121

a

b

Figure 22. Box-plot of dual-tasking lateral gastrocnemius muscle activity CON vs SVT during firm surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the lateral gastrocnemius muscle activity in the EOFS (a) and ECFS (b). No observed main effect of time for each group.

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a

b

Figure 23. Box-plot of dual-tasking lateral gastrocnemius muscle activity CON vs SVT during salt surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the lateral gastrocnemius muscle activity in the EOSS (a) and ECSS (b). No observed main effect of time for each group.

123

a

b

Figure 24. Box-plot of dual-tasking tibialis anterior muscle activity CON vs SVT during firm surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the m-CTSIB scores in the EOFS (a) and ECFS (b). No observed main effect of time.

124

a

b

Figure 25. Box-plot of dual-tasking tibialis anterior muscle activity CON vs SVT during soft surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the m-CTSIB scores in the EOSS (a) and ECSS (b) conditions. SVT group showed a main effect of time in the muscle activity of the tibialis anterior in the ECSS balance condition (p = 0.025; t = 2.674) (Figure 25b).

125

Dual-task motor cost

A 2x2 repeated measure ANOVA indicated that there was no interaction between the groups with the DT motor cost in all four conditions (EOFS: F =

0.038, df = 1, p = 0.848, Figure 26a; ECFS: F = 0.010, df = 1, p = 0.923,

Figure 26b; EOSS: F =0.523, df = 1, p = 0.479, Figure 27a; ECSS: F = 0.075, df = 1, p = 0.788, Figure 27b).

The eyes opened conditions showed a decrease in the post mean motor cost in the CON group (EOFS ↓ 25%, EOSS ↓44%) and an increase in the post mean motor cost in the SVT group (EOFS ↑ 32%, EOSS ↑ 185%) (Appendix

C. 4). The eyes closed conditions had an opposite pattern of increased motor cost in the CON group (ECFS ↑ 57%, ECSS ↑ 31%) and decreased motor cost in the SVT group (ECFS ↓ 10%, ECSS ↓ 20%) (Appendix C. 4).

126

a

b

Figure 26. Box plot of the dual-tasking motor cost CON vs SVT during firm surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the dual-tasking motor cost in the EOFS (a) and ECFS (b). No observed main effect of time for each group.

127

a

b

Figure 27. Box plot of the dual-tasking motor cost CON vs SVT during soft surface conditions

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the dual-tasking motor cost in the EOSS (a) and ECSS (b). No observed main effect of time for each group.

128

Dual-tasking Cognitive Cost

A 2x2 repeated measure ANOVA indicated that there was no interaction between the groups with the DT cognitive cost in all four conditions (EOFS: F

= 2.310, df = 1, p = 0.146, Figure 28a; ECFS: F = 0.330, df = 1, p = 0.573,

Figure 28b; EOSS: F =0.474, df = 1, p = 0.500, Figure 29a; ECSS: F = 1.376, df = 1, p = 0.256, Figure 29b).

Both groups had an observed decrease in post mean DT cognitive cost in all conditions except for unchanged cognitive cost in the EOFS for the SVT group. The CON group had the highest decrease in the firm surface conditions (EOFS ↓ 48%, ECFS ↓54%) and the SVT group had the highest decrease in the soft surface conditions (EOSS ↓ 59%, ECSS ↓58%)

(Appendix C. 5).

129

a

b

Figure 28. Box plot of the dual-tasking cognitive cost CON vs SVT during firm surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the dual-tasking cognitive cost in the EOFS (a) and ECFS (b) conditions. No observed main effect of time for each group.

130

a

b

Figure 29. Box plot of the dual-tasking cognitive cost CON vs SVT during soft surface conditions.

Central horizontal line in the box represents the median of the sample. Top line of the box if the upper quartile, bottom line is the lower quartile. Whiskers indicate values not within the top and lower quartiles. Top whiskers indicate the maximum value and the bottom whiskers the minimum value. The dots indicate outliers that are greater or less than 1.5 times the closest quartile range. No interaction between the groups with the dual-tasking cognitive cost in the EOSS (a) and ECSS (b) conditions. No observed main effect of time for each group.

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Discussion

Our aim for this study was to determine the effect of SVT on dual-tasking postural control and muscle activity in older adults. Our results did not indicate a significant effect of SVT on dual tasking postural balance from the m-CTSIB scores. The SVT also did not have a significant effect on the dual- tasking muscle activity during the m-CTSIB.

When comparing the single-task and dual-task change scores the CON group showed a negative change (lower postural sway) in the DT balance condition and the SVT group had a negative change score in mostly the ST balance conditions. This indicates that the backward counting mental task improved performance in the CON group but not the SVT group. Additionally, this effect was also observed in the DT ECFS condition in the SVT group. In other studies, dual-tasking has been shown to impair postural balance in older adults because of the competing attention demands (Brown et. al., 1999;

Shumway-Cook and Wollacott, 2000; Jamet et.al., 2004).

Maintaining postural balance while standing is an automatic process that usually does not require attention unless there are anticipated perturbations or challenging sensory inputs. During dual-tasking, attention was focused on the cognitive task and standing in different sensory conditions. The dual task of backward counting possibly removed the overt attention of just standing unlike in the single-task balance conditions. Other studies have also shown that incorporating external attention with dual tasking improves postural balance in older adults (McNevin et. al., 2003; Wulf et. al., 2004).

132

Visual input plays a role in postural balance by providing information about the body’s orientation to the environment. Stoffregen and colleagues (1999, 2000) demonstrated that dual tasking with visual fixation as a secondary task improves balance performance. Other studies have shown that postural balance was negatively affected when a secondary task involved processing of visual information (Kerr et. al., 1985; Maylor and Wing, 2001).

Our study indicated that the SVT group had a similar negative change score (lower postural sway) as the CON group in the DT ECFS condition. In this condition, visual sensory input is removed with the eyes closed thus there are less sensory inputs to integrate for postural balance. In normal single task standing, elimination of visual sensory input would impair postural balance but with our results it seems that less sensory inputs lessened the competition for attention and allowed for prioritization of maintaining postural balance.

This is further supported with the results of the motor cost and cognitive cost during the ECFS and ECSS balance conditions. The SVT did not result in a significant interaction between the CON and SVT groups with the dual tasking motor and cognitive cost, but our results did show an effect worth looking into.

The SVT showed a decrease in motor and cognitive cost in the ECSS balance conditions unlike the CON group which had an increase in the motor cost.

Even though the DT m-CTSIB did not show any significant interactions and effects following vibration therapy, calculating the motor cost from the single and dual task m-CTSIB sway index scores revealed a worth noting effect of the vibration therapy on the motor and cognitive costs.

133

The observed decrease in motor cost of the SVT could be an effect of the vibration therapy on the muscle activity and thus the sway index scores.

However, there was no observed major effect on the muscle activity during the dual-task m-CTSIB. The ECSS balance condition is the most challenging condition with all sensory input compromised or eliminated except for the vestibular sensory input.

Therefore, the improvement in both motor cost and cognitive cost in the

SVT group could be a result of less sensory inputs present and more attention focused on the mental task with less attention focused on the more automated task of standing. This would decrease the attentional demands of conscious sensory integration and help the participants perform better on the cognitive task with less conscious integration of the automated task of standing.

Another possible explanation for the improvement in both motor and cognitive cost in the SVT group following vibration therapy could be that the vibration therapy improved the sensitivity of the muscle spindles and golgi tendons.

The SVT group had a slight improvement in the motor cost in the ECFS and

ECSS balance conditions unlike the CON group which had an increased cost of more than 30% in both conditions. The improvement in sensitivity of the proprioceptive organs could have given the participants in the SVT group a better perception of the surface and integration of proprioceptive inputs when visual input was altered to improve their maintenance of postural sway and motor cost.

134

One of the limitations of this study is the use of serial subtraction of 3 as a secondary task for the dual-tasking balance assessment. The task required an oral response which has shown to worsen postural balance because it engages abdominal muscles which are also used during postural balance

(Yadley et. al., 1999; Dault et. al., 2003).

Conclusion

Our study did not show an effect of SVT on postural balance and muscle activity during dual tasking. However, our data suggests the vibration therapy to have produced beneficial effects by improving proprioceptive sensitivity in older adults which could have improved the proprioceptive input in challenging balance conditions when visual input was removed. This allowed for better integration of the available sensory input to maintain postural balance.

Further research and scrutiny are needed to confirm this effect of SVT.

Furthermore, our study confirmed the competition of attention resources and that when visual sensory input is removed, there is less sensory input to integrate, allowing for the direction of attention to more prioritized tasks and less focus on normally automated tasks like standing.

135

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V. SUMMARY CHAPTER

Postural control and balance involves the integration of sensory inputs within the central nervous system while coordinating and executing motor functions.

Balance is defined as the ability to maintain the body’s center of gravity over the base of support (Rogers et. al., 2005) and it involves the integration of visual, vestibular, proprioceptive and motor output of various muscles, including the lower limb and core muscles (Peterka et. al., 2002). These systems deteriorate in function with ageing which leads to a higher risk of falls

(Laughton et. al., 2003).

In an effort prevent falls in older adults, it is important to examine the potential benefits of balance improving interventions in clinical and community settings.

A new intervention that is independent of patient motivation and has been used in various clinical settings is vibration therapy (Rauch, 2009). Whole body vibration (WBV) has been shown to improve gait, motor function (Ridgel et.al., 2013) and leg muscle strength resulting in better balance and mobility in older adults (Lam et. al., 2012). The applied vibrations stimulate muscle spindles which activates alpha-motor neurons, and this initiates a muscle contraction (Cardinale and Bosco, 2003). WBV also promotes beneficial physiological effects such as improved oxygen uptake, blood flow, muscle strength, balance and postural control (Cardinale & Bosco, 2003; Cochrane et. al., 2008). Similarly, segmental vibration therapy (SVT), can be used to target vibration therapy to specific muscle groups. With a direct target to a muscle group of interest, participants receiving SVT can be in a seated

142 position and there will be minimum side effects from activation of other muscle of no interest or the whole body.

The increase in postural sway has been shown to be due to an age- related increase in muscle activity to maintain posture during quiet standing following the deteriorating sensory and neuromuscular control mechanisms

(Nagai et. al., 2012 and Laughton et. al., 2003). In normal circumstances, leg muscle co-activation has a stabilizing effect on short term postural sway

(Nagai et.al., 2011). However, there has been a shown increase in co- activation of antagonist muscle groups in older adults compared to young adults (Laughton et. al., 2003). This creates a negative correlation between postural sway and muscle co-activation. The increase in muscle activity and co-activation is a compensatory mechanism to increase joint stiffness and enhance stability (Nagai et.al., 2011). The change in muscle activity has been suggested to be a compensatory mechanism to the decrease in muscle strength with ageing (Woollacott et.al., 1990) and leg muscle strength highly correlates with balance and mobility (Lam et.al., 2012).

Our study indicated that SVT decrease muscle activity of the gastrocnemius in the EOSS and ECSS condition, and tibialis anterior in the ECFS and ECSS condition of the SVT group. These are the more challenging balance conditions because visual input is removed, and the proprioceptive input is challenged. Therefore, by directly applying the vibration therapy to the muscles, SVT modulated the compensatory increased muscle activation that is usually observed in older adults.

143

Cognitive functions such as executive function and attention are required to maintain balance during gait and standing (Smith-Ray et. al., 2013). With increasing age, cognitive function declines and motor tasks such as balance and walking become less automated and cognitively taxing (Schaefer and

Schumacher, 2011). In older adults, these changes result in difficulties performing a physical task while simultaneously completing a secondary cognitive task (dual tasking) (Laessoe et. al., 2008). Furthermore, older adults with cognitive impairments have an increased risk of falling (Herman et. al.,

2010; Holtzer et. al., 2007). The dual tasking deficit that is observed in older adults may be caused by the degradation of prefrontal cognitive processes

(Smith-Ray et. al., 2013).

WBV has shown to improve cognitive function, particularly inhibitory control as a measure of attention in adults with attention deficit hyperactivity disorder (ADHD) (Fuermaier et. al., 2014). Moreover, animal studies provide evidence of improved maze learning and enhanced neuronal activity in mice following whole body vibration (Keijser et. al., 2011).

This study did not show a significant improvement in executive function, specifically attention and inhibitory control, working memory and processing speed. It did however indicate that when visual input was removed in the

ECFS and ECSS conditions during dual tasking with a cognitive task, participants had less sensory inputs to integrate, which allowed them to focus

144 their attention on the cognitive tasks and less focus on normally automated tasks like standing. The SVT resulted in more than 50% improvement in cognitive cost in the soft surface conditions (EOSS and ECSS) during dual tasking. This suggests that the vibration therapy improved proprioceptive sensitivity resulting in better perception of the surface and integration of proprioceptive inputs.

In conclusion, SVT may be a valuable therapy to improve postural balance and reduce falls in older adults by decreasing muscle activation leading to less stiffness and improving proprioceptive sensitivity to allow for better perception of foot placement. Further research needs to be conducted to confirm the proprioceptive sensitivity and to determine the length of effect of the vibration therapy.

145

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APPENDICES

Appendix A: Effect of SVT on balance and muscle activity data tables.

Table A. 1. m-CTSIB sway index scores

CON (n=10) SVT (n=10) p value EOFS Pre: 0.42 ± 0.12 Pre: 0.40 ± 0.19 0.443 Post: 0.42 ± 0.21 Post: 0.34 ± 0.051

ECFS Pre: 0.69 ± 0.49 Pre: 0.67 ± 0.34 0.782 Post: 0.72 ± 0.67 Post: 0.63 ± 0.32

EOSS Pre: 0.82 ± 0.39 Pre: 0.89 ± 0.29 0.881 Post: 0.83 ± 0.27 Post: 0.72 ± 0.22

ECSS Pre: 2.79 ± 0.86 Pre: 3.03 ± 0.92 0.857 Post: 2.81 ± 1.17 Post: 2.72 ± 0.87

Data represented as mean ± SD.

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Table A. 2. Muscle activity (as percentage of MVC) during each balance condition CON vs SVT.

Muscle m-CTSIB CON (n=10) SVT (n=10) p Condition value Soleus EOFS Pre: 12.24 ± 8.38 Pre: 10.17 ± 5.73 0.418 Post: 12.75 ± 11.69 Post: 9.15 ± 6.38 ECFS Pre: 15.17 ± 15.77 Pre: 10.46 ± 5.57 0.542 Post: 17.62 ± 27.36 Post: 13.49 ± 11.42 EOSS Pre: 14.80 ± 13.97 Pre: 12.72 ± 6.37 0.777 Post: 15.77 ± 16.94 Post: 14.81 ± 10.39 ECSS Pre: 22.48 ± 24.83 Pre: 22.51 ± 12.27 1.0 Post: 23.04 ± 29.63 Post: 22.99 ± 18.37 Lateral EOFS Pre: 6.75 ± 5.02 Pre: 6.88 ± 4.84 0.113 Gastrocnemius Post: 8.36 ± 2.83 Post: 4.18 ± 2.24 ECFS Pre: 7.63 ± 5.38 Pre: 8.71 ± 7.80 0.112 Post: 11.29 ± 6.42 Post: 4.43 ± 2.21 EOSS Pre: 8.09 ± 4.63 Pre: 9.35 ± 6.75 0.122 Post: 11.24 ± 6.21 Post: 5.13 ± 1.99 ECSS Pre: 12.65 ± 8.01 Pre: 17.85 ± 18.20 0.506 Post: 18.65 ± 13.33 Post: 7.87 ± 5.17 Tibialis Anterior EOFS Pre: 2.59 ± 1.32 Pre: 3.87 ± 2.37 0.878 Post: 5.20 ± 6.25 Post: 3.56 ± 3.23 ECFS Pre: 3.14 ± 2.78 Pre: 7.53 ± 6.54 0.394 Post: 13.13 ± 16.45 Post: 3.66 ± 3.20 EOSS Pre: 3.21 ± 2.83 Pre: 5.58 ± 4.66 0.404 Post: 10.02 ± 16.43 Post: 3.15 ± 1.37 ECSS Pre: 12.33 ± 11.37 Pre: 27.77 ± 18.60 0.950 Post: 27.46 ± 26.69 Post: 11.31 ± 9.53 Data represented as mean ± SD.

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Appendix B: Effect of SVT on Executive function data tables.

Table B. 1. Attention and Inhibition scores.

CON (n=10) SVT (n=10) p value Computed scores Pre: 7.24 ± 0.71 Pre: 8.03 ± 0.44 0.061 Post: 7.51 ± 0.82 Post: 8.26 ± 0.46

Fully corrected Pre: 40.25 ± 6.27 Pre: 42.50 ± 4.04 0.367 T -scores Post: 42.00 ± 7.19 Post: 46.50 ± 5.45

Data represented as mean ± SD.

Table B. 2. Working memory scores.

CON (n=10) SVT (n=10) p value Raw scores Pre: 15.25 ± 2.32 Pre: 20.20 ± 3.03 0.042 Post: 17.25 ± 3.96 Post: 19.40 ± 2.07

Fully corrected Pre: 47.25 ± 8.14 Pre: 65.50 ± 7.51 0.041 T -scores Post: 54.00 ± 12.74 Post: 61.00 ± 6.73

Data represented as mean ± SD.

Table B. 3. Processing speed scores.

CON (n=10) SVT (n=10) p value Raw scores Pre: 34.25 ± 7.74 Pre: 43.60 ± 4.1 0.039 Post: 40.38 ± 8.52 Post: 48.80 ± 3.42

Fully corrected Pre: 39.25 ± 13.94 Pre: 53.00 ± 8.17 0.074 T -scores Post: 50.63 ± 15.07 Post: 66.75 ± 5.80

Data represented as mean ± SD.

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Appendix C: Effect of SVT on dual-tasking postural balance data tables

Table C. 1. Dual-task m-CTSIB sway index scores.

CON (n=10) SVT (n=10) p value EOFS Pre: 0.68 ± 0.28 Pre: 0.54 ± 0.25 0.612 Post: 0.56 ± 0.23 Post: 0.58 ± 0.26

ECFS Pre: 0.75 ± 0.55 Pre: 0.63 ± 0.23 0.477 Post: 0.77 ± 0.48 Post: 0.63 ± 0.28

EOSS Pre: 1.10 ± 0.18 Pre: 1.24 ± 0.75 0.438 Post: 1.00 ± 0.21 Post: 1.25 ± 0.84

ECSS Pre: 2.58 ± 0.88 Pre: 2.48 ± 0.86 0.975 Post: 2.54 ± 1.0 Post: 2.62 ± 1.21

Data represented as mean ± SD.

Table C. 2. Single-task vs. Dual-task m-CTSIB change scores.

CON (n=10) SVT (n=10) p value EOFS ST: 0.01 ± 0.16 ST: - 0.06 ± 0.16 0.408 DT: - 0.12 ± 0.15 DT: 0.04 ± 0.19

ECFS ST: 0.04 ± 0.23 ST: - 0.04 ± 0.32 0.515 DT: 0.01 ± 0.19 DT: - 0.01 ± 0.18

EOSS ST: 0.01 ± 0.19 ST: - 0.17 ± 0.28 0.745 DT: - 0.10 ± 0.28 DT: 0.01 ± 0.47

ECSS ST: 0.02 ± 0.59 ST: - 0.31 ± 0.61 0.722 DT: - 0.04 ± 0.45 DT: 0.14 ± 0.51

Data represented as mean ± SD.

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Table C. 3. Muscle activity during dual-tasking m-CTSIB.

Muscle m-CTSIB CON (n=10) SVT (n=10) p Condition value Soleus EOFS Pre: 13.41 ± 10.14 Pre: 11.59 ± 6.05 0.562 Post: 12.82 ± 10.18 Post: 10.51± 5.20 ECFS Pre: 15.33 ± 14.30 Pre: 11.80 ± 6.36 0.432 Post: 17.04 ± 20.70 Post: 11.40 ± 5.62 EOSS Pre: 15.69 ± 12.56 Pre: 14.66 ± 6.99 0.974 Post: 15.01 ± 12.83 Post: 16.34 ± 7.08 ECSS Pre: 21.99 ± 20.91 Pre: 21.29 ± 12.58 0.865 Post: 23.71 ± 29.45 Post: 21.39 ± 11.44 Lateral EOFS Pre: 6.82 ± 4.78 Pre: 8.4 ± 4.91 0.160 Gastrocnemius Post: 5.38 ± 3.14 Post: 9.59 ± 5.56 ECFS Pre: 7.59 ± 5.13 Pre: 8.81 ± 6.62 0.278 Post: 6.45 ± 3.36 Post: 10.94 ± 8.28 EOSS Pre: 8.11 ± 4.90 Pre: 13.60 ± 12.05 0.159 Post: 6.84 ± 3.23 Post: 12.06 ± 10.01 ECSS Pre: 12.19 ± 6.62 Pre: 17.33 ± 16.04 0.287 Post: 9.78 ± 4.62 Post: 15.64 ± 14.24 Tibialis Anterior EOFS Pre: 2.89 ± 1.46 Pre: 5.54 ± 6.31 0.349 Post: 4.11 ± 3.17 Post: 5.00 ± 4.77 ECFS Pre: 3.49 ± 2.66 Pre: 5.74 ± 5.48 0.260 Post: 4.80 ± 4.04 Post: 8.30 ± 10.91 EOSS Pre: 4.24 ± 3.42 Pre: 8.01 ± 6.57 0.110 Post: 4.53 ± 2.54 Post: 13.12 ± 16.46 ECSS Pre: 10.79 ± 9.73 Pre: 18.29 ± 15.38 0.153 Post: 11.41 ± 8.77 Post: 22.49 ± 20.17 Data represented as mean ± SD.

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Table C. 4. Dual-task motor cost (%).

CON (n=10) SVT (n=10) p value EOFS Pre: 69.74 ± 59.97 Pre: 56.60 ± 48.46 0.848 Post: 52.02 ± 57.51 Post: 74.68 ± 78.30

ECFS Pre: 33.58 ± 24.24 Pre: 39.77 ± 47.75 0.923 Post: 52.76 ± 52.11 Post: 43.78 ± 41.12

EOSS Pre: 63.26 ± 56.08 Pre: 41.54 ± 52.27 0.479 Post: 35.67 ± 22.69 Post: 118.33 ± 212.78 ECSS Pre: 13.32 ± 13.66 Pre: 18.67 ± 14.47 0.788 Post: 17.50 ± 10.00 Post: 14.88 ± 14.44

Data represented as mean ± SD.

Table C. 5. Dual-task cognitive cost (%).

CON (n=10) SVT (n=10) p value EOFS Pre: 41.94 ± 21.69 Pre: 23.95 ± 18.74 0.146 Post: 21.70 ± 20.31 Post: 24.64 ± 16.37

ECFS Pre: 45.11 ± 39.13 Pre: 43.82 ±44.47 0.573 Post: 20.89 ± 25.24 Post: 33.85 ± 25.93

EOSS Pre: 31.98 ± 33.48 Pre: 48.28 ± 58.30 0.500 Post: 21.09 ± 20.24 Post: 19.70 ± 14.25

ECSS Pre: 38.13 ± 32.98 Pre: 66.58 ± 73.57 0.256 Post: 23.43 ± 22.30 Post: 28.17 ± 25.00

Data represented as mean ± SD.

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