Abnormal muscle activity during balance before and after an exercise-based balance rehabilitation in people with Parkinson’s disease Open Access

Abstract

BACKGROUND: Abnormal muscle activity during reactive balance may cause balance impairments in Parkinson’s disease (PD) and may be a potential mechanism by which Adapted Tango (AT), an exercise-based balance rehabilitation intervention, improves clinical balance measures. Here, a multidirectional perturbation paradigm was used to quantify how antagonist muscle activity during reactive balance is influenced by 1) PD and impaired balance assessed by standardized behavioral scales and 2) AT. METHODS: Antagonist activation during reactive balance responses to multidirectional support-surface translation perturbations was compared between 1) 31 participants with PD and 13 participants without PD and 2) 30 participants with PD who did (16) or did not (14) participate in AT. Muscle modulation (the ability to activate and inhibit muscles appropriately according to perturbation direction) was quantified using modulation indices (MI, MI180) derived from minimum and maximum EMG activation levels observed across perturbation directions. Modulation was quantified for 100-175 ms (APR1), 70-450 ms (APRX), and 175-250 ms (APRY) after perturbation onset. Clinical measures quantified balance (Berg Balance Scale, BBS; Fullerton Advanced Balance scale, FAB) and gait (Dynamic Gait Index, DGI) performance. RESULTS: In cross-sectional comparisons using MI and APRX, antagonist leg muscle activity was abnormal in participants with PD compared to participants without PD. Linear mixed models identified significant associations between impaired modulation and PD (P<0.05), PD severity (P<0.01), and balance ability (P<0.05), but not age (P=0.10). In the longitudinal examination of AT or Control participants with PD, there was a significant group by time interaction effect on DGI performance, but not on BBS or FAB. Neither the group, time, nor group by time interaction effects were significant for MI in either APRX or APRY. Individual cases showed relationships between FAB and MI changes differing with baseline balance ability. CONCLUSION: This dissertation 1) presents a new method to quantify co-contraction, 2) shows that reduced modulation is associated with PD severity and across PD phenotypes, and with clinical quantifications of balance, and 3) provides evidence suggesting that baseline functional balance ability may be more important to rehabilitation outcomes than age or PD phenotype, with those who stand to benefit most having lower balance ability.

Table of Contents

Table of Contents

List of Abbreviations....................................................................................................................... 1

1.   Introduction............................................................................................................................ 2

1.1.  Parkinson’s disease impairs balance............................................................................. 2

1.2.  Multiple mechanisms contribute to successful balance and are affected by Parkinson’s disease 3

1.3.  Impaired balance is tested with perturbations in both the clinic and laboratory............ 5

1.4.  Perturbation-induced reactive balance responses allow quantification of muscle coordination during automatic postural responses   6

1.5.  Automatic postural responses offer a probe into the neural substrates of balance......... 9

1.6.  Parkinson’s disease may impair balance-restoring automatic postural responses through muscle co-contraction        10

1.7.  Rehabilitation interventions have been shown to improve balance in Parkinson’s disease         12

1.8.  Rehabilitation interventions have been shown to improve muscle activity patterns in Parkinson’s disease        14

1.9.  This work uses electromyography to probe mechanisms of balance impairment and improvement        14

1.10. This work presents a new method for assessing muscle modulation............................ 15

2.   Antagonist muscle activity during reactive balance responses is elevated in Parkinson’s disease and in balance impairment       17

2.1.  Abstract......................................................................................................................... 17

2.2.  Introduction................................................................................................................... 18

2.3.  Methods......................................................................................................................... 19

2.3.1  Participants........................................................................................................ 19

2.3.2  Assessment protocol........................................................................................... 20

2.3.3  Reactive balance assessments.............................................................................. 21

2.3.4  EMG processing.................................................................................................. 23

2.3.5  Muscle activity modulation indices: MI and MI180............................................. 23

2.3.6  Statistical Analysis.............................................................................................. 25

2.4.  Results........................................................................................................................... 27

2.4.1  Participant characteristics................................................................................... 27

2.4.2  Description of muscle activity across perturbation directions.............................. 29

2.4.3  PD, age, and impaired balance ability were associated with impaired modulation in some individual muscles 29

2.4.4  PD, PD severity, and impaired balance ability were associated with impaired modulation across muscles     31

2.5.  Discussion..................................................................................................................... 32

2.6.  Appendix: Antagonist muscle activity during reactive balance responses is elevated in Parkinson’s disease and in balance impairment.         36

2.6.1  Additional linear mixed models........................................................................... 36

2.6.2  Interaction between PD and age.......................................................................... 36

2.6.3  PD phenotype.................................................................................................... 37

2.6.4  PD severity......................................................................................................... 37

2.6.5  Associations between study variables and modulation indices in APR1................. 38

3.   People with PD and high baseline balance function do not improve on clinical measures of balance or abnormal antagonist muscle activity after completion of an Adapted Tango intervention.......................................... 39

3.1.  Abstract......................................................................................................................... 39

3.2.  Introduction................................................................................................................... 40

3.3.  Methods......................................................................................................................... 42

3.3.1  Study design........................................................................................................ 42

3.3.2  Participants........................................................................................................ 42

3.3.3  Adapted Tango Intervention............................................................................... 44

3.3.4  Outcome measure assessment.............................................................................. 45

3.3.5  Reactive balance assessment................................................................................ 46

3.3.6  EMG collection and processing........................................................................... 46

3.3.7  Muscle activity modulation index (MI)............................................................... 46

3.3.8  Statistical analysis............................................................................................... 47

3.4.  Results........................................................................................................................... 48

3.4.1  Baseline participant characteristics..................................................................... 48

3.4.2  Adapted Tango participation and assessment timing........................................... 50

3.4.3  Effect of Adapted Tango on clinical outcome measures...................................... 50

3.4.4  Effect of Adapted Tango on muscle modulation.................................................. 51

3.5.  Discussion..................................................................................................................... 53

4.   Changes in muscle modulation during reactive balance and in clinical measures of balance after Adapted Tango depend on baseline balance ability: A case series............................................................................................. 57

4.1.  Abstract......................................................................................................................... 57

4.2.  Introduction................................................................................................................... 58

4.3.  Methods......................................................................................................................... 59

4.4.  Results........................................................................................................................... 61

4.4.1  Baseline Characteristics and Clinical Presentation............................................... 61

4.4.2  Change in balance ability and muscle modulation after Adapted Tango................ 61

4.5.  Conclusion.................................................................................................................... 64

4.6.  Discussion..................................................................................................................... 64

5.   Discussion............................................................................................................................. 66

5.1.  Overview....................................................................................................................... 66

5.2.  New methodology for assessing co-contraction............................................................ 66

5.3.  Muscle modulation is decreased in people with PD and associated with PD severity and balance ability           67

5.4.  Neither muscle modulation nor balance ability changed significantly after Adapted Tango in a group of participants with high baseline balance ability............................................................................................................................. 69

5.5.  Effects of modulation levels may differ based on balance ability................................... 70

5.6.  Parkinson’s disease, symptom severity, and balance ability are related to abnormal antagonist activation and how changes in that activation relate to functional balance control............................................................................... 71

5.7.  Limitations.................................................................................................................... 72

5.8.  Implications for future studies....................................................................................... 73

5.9.  Co-contraction: Helpful or harmful in Parkinson’s disease?....................................... 75

5.10. Co-contraction: Cause and effect of balance impairment? What effect should rehabilitation have on co-contraction?   76

5.11. Summary....................................................................................................................... 78

6.   References............................................................................................................................. 79

About this Dissertation

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School	Laney Graduate School
Department	Biological and Biomedical Sciences
Subfield / Discipline	Neuroscience
Degree	Ph.D.
Submission	Dissertation
Language	English
Research Field	Biology, Neuroscience Health Sciences, Rehabilitation and Therapy
Keyword	Balance Electromyography Rehabilitation Posture Parkinson's disease Antagonist activity Muscle
Committee Chair / Thesis Advisor	Ting, Lena, Emory University
Committee Members	McKay, J. Lucas, Emory University Wichmann, Thomas, Emory University Wolf, Steven, Emory University Hackney, Madeleine, Emory University

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