Customized interactive graphical analysis programs (MatLab 6.0, MathWorks Inc., Natick, MA) were used to compute the temporal and spatial characteristics of the APAs and initial stepping responses. As described in previous reports,14,16,22 the lateral APA is characterized by an initial displacement of the net COP toward the first step side that propels the body's COM laterally toward the side of the single support limb. At the same time, a posterior shift in the COP propels the body forward in the direction of stepping. An unloading of the step limb and continuous upward and forward displacement of the foot represents the beginning of the step cycle.
Ground reaction forces were recorded to calculate the net mediolateral (ML) COP displacement recorded beneath both feet from which the characteristics of the APA (duration and amplitude) were determined. The APA onset was identified when the COP began ML displacement toward the first step foot (when the first derivative of lateral COP is not 0) (ie, the onset of the lateral weight transfer). The APA duration occurred between APA onset time and the instant when the lateral COP reached maximum displacement toward the single stance side before step liftoff (ie, the end of the lateral weight transfer). The APA amplitude corresponded to the maximum stepping side lateral COP displacement.
The first step characteristics (onset, duration, and length) were derived from the motion of the preferred step limb ankle marker. The step onset time was determined relative to the instant of the initial lateral COP change from baseline, ie, APA onset. The duration was defined from the beginning and end of the step as indicated by the vertical velocity of the ankle marker. Step length was assessed as the displacement of the ankle between step onset and end in the forward direction.
Mean values were determined for all subjects and variables. A mixed-model repeated-measures analysis of variance was used to assess between-group differences (participants with PD and healthy controls) and within-group differences (baseline, acquisition, immediate retention, and one-week retention).33 The 50 acquisition trials with the lateral assist were divided into five blocks of 10 trials (A1–A5). To assess possible differences in performance between early trials (early acquisition) and late trials (late acquisition), A1 and A5 trial blocks were analyzed. Similarly, earlier and later immediate retention performances were represented by the means of trials 1 to 3 (early immediate retention) and trials 7 to 10 (late immediate retention). In cases of significant analysis of variance main effects or interactions, planned post hoc analyses were performed using paired t tests with the level of significance adjusted for multiple comparisons using a Bonferroni correction.34 For all comparisons, a significance level was set at P < 0.05.
Across all conditions, the participants with PD had longer APA durations than controls (P < 0.03) (Fig. 3A). There was a significant main effect of condition (P < 0.001) whereby APA duration was shorter (P < 0.001) for both early acquisition (P < 0.001) and late acquisition (P < 0.001) trials compared with baseline trials indicating that the assist did improve subjects' lateral weight transfer. The duration of the APA did not differ significantly (P > 0.05) between baseline and retention conditions. There was no significant group by condition interaction.
Although the participants with PD generally tended to initiate the first step relative to APA onset later than healthy control individuals, there was no significant between subject effect for the step onset time (P = 0.11) (Fig. 3B). A significant within-subject effect (P < 0.001) indicated that, compared with the baseline condition, the mean step onset time occurred 104 (early acquisition) and 98 milliseconds (late acquisition) earlier for the participants with PD, and 84 (early acquisition) and 62 milliseconds (late acquisition) earlier for the healthy controls (P < 0.001). Retention trials were not statistically different from baseline trials.
During step execution, there were no significant between-group effects or within-group effects for first step length (Fig. 3C). However, first step duration (Fig. 3D) was generally longer (P < 0.04) across all the conditions for participants with PD compared with controls. Compared with the baseline condition, a significant within-group effect (P < 0.001) also indicated that step duration became shorter across the groups especially during the late acquisition trials (P = 0.002). Furthermore, this shorter step duration persisted during both immediate retention (P < 0.001) and one-week retention (P < 0.001) trials.
The purpose of this study was to determine the short-term effects of a single session of repetitive robotic assistance training with the APA on rapid step initiation in participants with PD in the medications “on” condition and healthy control subjects. The results expand on the observations of our previous study22 and further demonstrated the persistence of the acute effects of posture assistance on the temporal aspects of stepping performance over a series of 50 trials. The finding that the speed of first step execution remained faster than baseline immediately after posture assistance was removed, and for up to one-week post-training, suggested retention of improvements in the temporal aspects of stepping affecting bradykinetic movement.
Influence of Posture Assistance on Rapid Step Initiation
As in past studies,10,20–22 participants with PD in the medication “on” state had a longer APA duration reflecting a postural deficit and took longer to execute the first step than healthy control subjects. The PD group also showed a general tendency for the timing sequence or temporal coordination between APA onset and step onset to be slightly longer than for controls, but this trend was not statistically different for these mildly to moderately involved individuals.
The application of a precisely timed lateral waist pull introduced in the early phase of self-triggered ML APAs, shortened the APA duration for lateral weight transfer. Compared with an earlier study22 showing that APA duration is reduced from unassisted baseline performance with lateral postural assistance during a block of only six trials, the current study results demonstrated that comparable effects persisted across a nearly fivefold increase in trial repetitions. Thus, posture-assisted changes in APA performance are sustainable at dosage levels of 40 to 60 trials that have been previously found to promote short-term acquisition of APAs during bimanual load lifting.35
Furthermore, the current postural effects were accompanied by earlier step initiation onset times and faster execution times for both participants with PD and healthy controls, which also persisted over the extended acquisition trial blocks. The APAs enhance whole-body balance stabilization before and during the first step and thus potentially affect frontal plane balance control and first step ML foot placement, distance, and timing.36 Thus, one might have expected a change in the step length with the postural assistance. However, this parameter was neither changed with the postural assistance nor different between the groups. The absence of a deficit in step length for these moderately affected participants with PD probably accounts for the absence of step-length modification.
Capacity for Adaptive Improvements in Stepping with Posture-Assisted Training in PD
Although it is known that individuals with PD can improve the speed, accuracy, and coordination of some motor tasks with task-specific practice,35,37 the achieved benefits are generally less pronounced or take longer to acquire than for healthy control subjects.35,37–40 However, this indicates that participants with PD generally retain the capacity to improve aspects of movement performance through practice training. For example, recent studies found that body weight–supported treadmill training in participants with PD can improve gait speed, stride length, and cadence immediately after a single session of training.40,41 Therefore, we reasoned that a single session of more intensive posture-assisted step training would result in immediate and short-term retention. Despite significant acquisition effects for APA duration and first step onset time, these changes were not retained. Thus, more intensive and long-term posture-assistance training may be required to produce more persistent changes. In contrast, however, first step duration, which was reduced during acquisition trials in both groups, remained significantly shorter during both immediate-retention and one-week retention trials. Because first step length was not different from baseline for any of the conditions, the subjects' first step speed was therefore faster for both groups in the same proportions.
Possible Mechanisms for Improvements in Step Initiation with Posture Assistance
Concerning the mechanisms through which improvements in posture and stepping components of step initiation may be achieved with posture assistance, it is possible that the pulling stimulus served as an external timing cue that enhanced performance. It is known, for example, that difficulty in executing particularly internally cued voluntary movements is most problematic in PD and that such movements can be improved by the presentation of external sensory cues.1,6,20,21,42,43 External cueing has been proposed to bypass the neural pathways involving the disrupted basal ganglia output to the supplementary motor area of the cortex, which is thought to provide internal timing information for sequencing internally triggered motor subtasks.44 In a previous study,22 we compared posture-assist trials with a waist-tug condition that was delivered at the same location with the same timing (ie, pull onset and velocity) but used a displacement that was reduced to 25% of the acquisition waist pulls. The waist tug gave little mechanical assistance with lateral weight transfer but provided a vigorous stimulus to the pelvic area that could conceivably have been used as a timing cue to initiate stepping. No differences in the APA and stepping variables were found between baseline trials and waist-tug trials regardless of whether the waist tug immediately preceded or followed posture-assisted trials. Although the waist tug was likely a less intense stimulus than the posture-assist condition, subjects clearly perceived the waist-tug stimulus. In addition, healthy older control subjects, whose putative internal timing cue mechanism was presumably relatively intact, also improved their performance with posture assistance but not with the waist tug. Thus, the assistance with achieving anticipated postural state conditions involving the position and motion of the COM relative to the changing base of support configuration, more likely contributed to the faster onset timing of the gait cycle than the mere presence of an external timing cue.
It is also possible that the predictable timing delivery of the lateral waist pull during the APA performance helped subjects to better focus their attention on task performance.44 Alternatively, the imposition of the waist pull assist concurrent with subjects' efforts to initiate stepping might also have distracted their attention from the goal intended task. The current study does not rule out the former possibility but argues against task interference.
Although we did not specifically examine whether step practice without postural assistance might account for the present findings, a previous investigation suggested that the effects of the acquisition condition were not likely attributable to practice alone.22 In that study, when blocks of trials without postural assistance immediately followed acquisition trials that demonstrated improved APA and step characteristics over baseline, the unassisted trials did not vary from baseline. Hence, strict practice effects were not apparent. However, it might be that the increased number of trial repetitions used in the current study was more compatible with practice related improvements in performance.
Limitations of the Study
Among the limitations of this study is the focus on participants with early-stage PD, so that the findings may not be generalizable to individuals with more severe disease. The use of a relatively small sample size might have masked potential carryover effects of posture-assisted training on APA and stepping performance. There is a need to identify whether comparable or more robust changes in stepping performance can be achieved for more severely affected participants demonstrating greater deficits in posture and gait performance including freezing of gait. Another limitation was that participants with PD were only tested in the medications “on” state. Although the current study results were similar to those of a previous study22 involving comparably involved participants with PD tested in the medications “off” state, it would be important to know the extent to which such adaptive changes in stepping performance are dependent on dopaminergic mechanisms by directly comparing the effects of training in the medications “on” and “off” conditions for the same group of subjects. A further limitation is the need to more directly determine the extent to which practice training without postural assistance might contribute to the results. Furthermore, the retention effects on step execution timing found after a single training session might not be comparable during a longer training period. It also remains to be determined whether a long-term postural assistance intervention approach can lead to persistent improvements in gait initiation performance in individuals with PD.
In summary, the results of this study indicated that short-term acquisition improvements in temporal aspects of rapid gait initiation, including a shorter APA duration, earlier first step onset time, and shorter first step duration, are possible with a single session of posture-assisted step training in people with mild to moderate PD studied in the medications “on” state. It is encouraging that the adaptive changes in the speed of stepping were retained immediately and for as long as one week after training. This indicates that the capacity of participants with PD to potentially benefit from more intensive longer duration posture-assisted training.
The contributions of J. Spears, K. Ryczek, S, Shumacher, and A. Orzel to this project are gratefully acknowledged.
1. Martin JP. The Basal Ganglia and Posture.
Philadelphia: Lippincott; 1967.
2. Rogers MW. Disorders of posture, balance, and gait in Parkinson's disease. Clin Geriatr Med
3. Bonnet AM, Loria Y, Saint-Hilaire MH, et al. Does long-term aggravation of Parkinson's disease result from nondopaminergic lesions? Neurology
4. Grimbergen YA, Munneke M, Bloem BR. Falls in Parkinson's disease. Curr Opin Neurol
5. Krack P, Batir A, Van Blercom N, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med
6. Rubinstein TC, Giladi N, Hausdorff JM. The power of cueing to circumvent dopamine deficits: a review of physical therapy treatment of gait disturbances in Parkinson's disease. Mov Disord
7. Simuni T, Martinez KM, Rogers MW. Physical and occupational therapy in Parkinson's disease. In: Pahwa R, Lyons K, Koller WC, eds. Therapy of Parkinson's Disease
. New York: Marcel Dekker, Inc; 2004:481–490.
8. Deane KH, Jones D, Ellis-Hill C, et al. A comparison of physiotherapy techniques for patients with Parkinson's disease. Cochrane Database Syst Rev
9. Bloem BR, Hausdorff JM, Visser JE, et al. Falls and freezing of gait in Parkinson's disease: a review of two interconnected, episodic phenomena. Mov Disord
10. Crenna P, Giovannelli P, Piccolo I. The initiation of gait in Parkinson's disease. In: Berardelli A, Benecke R, Manfredi M, et al, eds. Motor Disturbances II
. London: Academic Press; 1990:161–173.
11. Brunt D, Lafferty MJ, Mckeon A, et al. Invariant characteristics of gait initiation. Am J Phys Med Rehabil
12. Carlsoo S. The initiation of walking. Acta Anat (Basel)
13. Crenna P, Frigo C. A motor programme for the initiation of forward-oriented movements in humans. J Physiol
14. MacKinnon CD, Bissig D, Chiusano J, et al. Preparation of anticipatory postural adjustments prior to stepping
. J Neurophysiol
15. Mann RA, Hagy JL, White V, et al. The initiation of gait. J Bone Joint Surg Am
16. Rogers MW, Kukulka CG, Brunt D, et al. The influence of stimulus cue on the initiation of stepping
in young and older adults. Arch Phys Med Rehabil
17. Massion J. Movement, posture and equilibrium: interaction and coordination. Prog Neurobiol
18. Massion J, Alexandrov A, Frolov A. Why and how are posture and movement coordinated? Prog Brain Res
19. Jian Y, Winter DA, Ishac MG, et al. Trajectory of the body COG and COP during initiation and termination of gait. Gait Posture
20. Burleigh-Jacobs A, Horak FB, Nutt JG, et al. Step initiation in Parkinson's disease: influence of levodopa and external sensory triggers. Mov Disord
21. Gantchev N, Viallet F, Aurenty R, et al. Impairment of posturo-kinetic co-ordination during initiation of forward oriented stepping
movements in parkinsonian patients. Electroencephalogr Clin Neurophysiol
22. Mille ML, Johnson Hilliard M, Martinez KM, et al. Acute effects of a lateral postural assist on voluntary step initiation in patients with Parkinson's disease. Mov Disord
23. Vaugoyeau M, Viallet F, Mesure S, et al. Coordination of axial rotation and step execution: deficits in Parkinson's disease. Gait Posture
24. Goulart FR, Valls-Sole J. Patterned electromyographic activity in the sit-to-stand movement. Clin Neurophysiol
25. Morris ME. Movement disorders in people with Parkinson disease: a model for physical therapy. Phys Ther
26. Pai YC, Rogers MW. Segmental contributions to total body momentum in sit-to-stand. Med Sci Sports Exerc
27. Pai YC, Rogers MW. Speed variation and resultant joint torques during sit-to-stand. Arch Phys Med Rehabil
28. Pai Y-C, Rogers MW. Control of body mass transfer as a function of speed of ascent in sit-to-stand. Med Sci Sports Exerc
29. Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology
30. Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res
31. Winter DA. Biomechanics and Motor Control of Human Gait
. Waterloo, Ontario: University of Waterloo Press; 1987.
32. Pidcoe PE, Rogers MW. A closed-loop stepper motor waist-pull system for inducing protective stepping
in humans. J Biomech
33. Toothaker LE, Newman D. Nonparametric competitors to the two-way ANOVA. J Educ Behav Stat
34. Portney LG, Watkins MP. Foundations of Clinical Research: Applications to Practice
. 2nd ed. Upper Saddle River, NJ: Prentice Hall, Inc.; 2000.
35. Massion J, Ioffe ME, Schmitz C, et al. Acquisition of anticipatory postural adjustments in a bimanual load-lifting task: normal and pathological aspects. Exp Brain Res
36. Lyon IN, Day BL. Control of frontal plane body motion in human stepping
. Exp Brain Res
37. Agostino R, Sanes JN, Hallett M. Motor skill learning in Parkinson's disease. J Neurol Sci
38. Behrman AL, Cauraugh JH, Light KE. Practice as an intervention to improve speeded motor performance and motor learning in Parkinson's disease. J Neurol Sci
39. Krebs HI, Hogan N, Hening W, et al. Procedural motor learning in Parkinson's disease. Exp Brain Res
40. Pohl M, Rockstroh G, Ruckriem S, et al. Immediate effects of speed-dependent treadmill training on gait parameters in early Parkinson's disease. Arch Phys Med Rehabil
41. Frenkel-Toledo S, Giladi N, Peretz C, et al. Treadmill walking as an external pacemaker to improve gait rhythm and stability in Parkinson's disease. Mov Disord
42. Dibble LE, Nicholson DE, Shultz B, et al. Sensory cueing effects on maximal speed gait initiation in persons with Parkinson's disease and healthy elders. Gait Posture
43. Jiang Y, Norman KE. Effects of visual and auditory cues on gait initiation in people with Parkinson's disease. Clin Rehabil
44. Morris ME, Huxham FE, McGinley J, et al. Gait disorders and gait rehabilitation in Parkinson's disease. Adv Neurol
Keywords:© 2009 Neurology Section, APTA
Parkinson's disease, posture; stepping; therapeutic training