This study investigated the motor learning dynamics of the postural control in people with PD, using the unidimensional measures of stability and flexibility degree that we proposed in a previous study [30]. The pattern of improvements during a 6-week balance-training program in people with PD was assessed. The evaluated outcomes comprised clinical measures of functional balance and mobility, posturography measures, and parameters of a patient-specific postural control model (particularly, the stability – KP –, and flexibility degree – Kn). Findings demonstrated that the balance-training program resulted in continuous improvements in mobility- and flexibility-related measures such as TUG, 6MWT, Tinetti gait score; as well as MV and Kn (flexibility degree), which changed significantly in R-tasks. Furthermore, balance- and stability-related measures – timed tandem stance with eyes open, step test, Tinetti balance score as clinical measures; f95, ∆tc, RMS on foam, KP (stability degree) as posturographic and model-based measures – showed an early improvement, in F-tasks, and reached a plateau before the end of the training program. The present study proposed a systematic approach to study the impact of specific training programs on postural disabilities in PD; and as such facilitates the design of new individualized and optimal interventions.
The found improvement at mid-training, and from mid- to post-training for clinical measures of functional mobility implies a relatively constant improvement in mobility. Esculier et al. [24] also observed a continuous reduction in TUG for people with PD, at mid-training (week 3) and post-training (week 6) during an 18-session balance training. Improved TUG even after short-term interventions [31, 32], supports the possibility that TUG (i.e. mobility) in PD can improve rapidly. Furthermore, the abrupt and ongoing improvement of gait performance in people with PD was documented with excessively short gait trainings, besides long-term trainings with multi-assessment design. For instance, a minimum of 2-week gait training promoted walking speed and gait performance [15, 33]. In addition, continuing increase in walking capacity – 6MWT –, using multiple assessments during 24 weeks of treadmill training in PD was observed [26]. This improvement, however, was not restricted to gait trainings; rather, short-term strength training [17] or resistance training [34] also caused increase in 6MWT in PD. At the same time, there exist studies, which found no improvement in mobility measures, even after long-term interventions due to high initial values that measures had at baseline or the unfocused, non-specific type of training that was applied [35, 36]. Considering the pivotal role that additional factors like type and duration of interventions play, the above-mentioned conjecture cannot be generalized.
Our findings on clinical balance tests suggest an early improvement (at mid-training) in postural stability, with subsequent plateaued behavior for the rest of the balance-training program. Such behavior – Saturation pattern – was in part, consistent with the results of a few studies, which included a mid-training assessment during a training program [24, 25]. For instance, Esculier et al. [24] reported improvements at mid-training for Tinetti total score, which remained almost the same to the end of the balance training. Unfortunately, none of these articles clearly reported whether a statistically significant change occurred from mid- to post-training; hence, complicating the differentiation between Saturation and Continuous pattern in the second half of program. In the same manner, Ganesan et al. [25] found improvements at mid- (session 8) and post-training (session 16) in Tinetti balance score. However, this improvement was 24.5% up to mid-training and merely 12% from mid- to post-training; suggesting a plateauing form in the second half of the training program (again not statistically tested). As a more objective test of balance, Stankovic [37] asserted that step test and tandem/one-leg stance more precisely discriminate the balance disorder in PD. We found no previous study, which investigated the mid-training changes in either step test or timed tandem stance. However, in a study by Nieuwboer et al. [38], Tandem-EO improved almost to its maximum score, following a minimum of 9 sessions (3 weeks) cueing training (as equal duration and sessions as our mid-training), which favors our results on early improvement of balance scores at mid-training. One may suspect that the Saturation pattern seen in these clinical scales might be the consequence of a natural ceiling effect. However, as for step test, a capability of up to 25 taps was recorded for healthy subjects (not shown here), implying that saturation in step test at 17 taps for PD patients (Table 1) was caused by the limited learning capacity in PD and not the ceiling effect in the assessment measure. Although most balance tests exhibited early-improvement followed by saturation, few balance tests behave differently. FRT showed a Continuous pattern. It is plausible that clinical scales like FRT are in fact assessing multiple tangled aspects of postural control, i.e. balance (or stability) and mobility (or in particular flexibility); considering the proven significant contribution of axial flexibility in FRT [16]. This may reiterate that the commonly used clinical tests have potential shortcomings such as being insensitive [4, 23], being multidimensional in measuring a mixture of contributors to postural control [8, 19], being confined by ceiling effects [39, 40], and being poorly defined in the level of the underlying constructs [8]. All these facts highlight the need to re-define current clinical measures.
Despite the equivocal results that may arise from clinical scales, the consistent set of postural sway measures along with the proposed model-based measures (stability and flexibility degree), provided clear conforming results. Findings revealed a constant improvement in flexibility-related measures, and early-progressed with plateaued behavior for stability-related measure. The increment in MV and Kn (flexibility degree) in R-tasks was characterized by a continuous improvement throughout sessions; nevertheless, it appeared significant almost late – only at week 6. Esculier et al. [24] also reported late improvement in MV, only at the end of the 6-week balance-training program. Interestingly, similar to our finding, MV in EC condition hardly improved as compared to EO condition [24]. Moreover, PD patients showed an accumulating capacity to improve the upper extremity movement velocity over a longer course of training (two-year progressive resistance training – PRE) [41]; suggesting the potential in flexibility and range-of-motion (ROM) features to improve continuously. Although both mobility- and flexibility-related measures exhibited a continuous progression, results indicated that flexibility, in contrast to mobility, reached significant changes at later times. Mobility advances sooner, likely because commuting to the rehabilitation center and participating in trainings, in turn, develop the physical and psychological well-being. In fact, the early improvement in mobility may be attributed to leaving the sedentary lifestyle; but its further improvement may be due to the gradual progression in other root factors such as flexibility. Nicely, Shen et al. [42] noticed that patients who dropped out a training program had lower mobility in comparison to non-dropout ones. Whilst usual exercise guidelines (e.g. by American College of Sport Medicine – ACSM) emphasize on longer exercise duration to achieve sustained improvements in flexibility [4] (at least 6 weeks [15]), a minimum of two [33] to four weeks [23] intervention turned out to be sufficient to enhance mobility. It is noteworthy that flexibility-related measures were mainly reflected in R-tasks, although other stability-related measures (such as f95 and KP) also showed modest improvement in R-tasks. Conversely, improved stability in the patients was mainly reflected in stability-related measures in F-tasks since these tasks challenge the stability more intensively.
The pattern of stability-related measures (f95, ∆tc, KP, RMS) in F-tasks was characterized by two main features: first, an early improvement during the first four weeks of training, and then a plateaued behavior in the remaining two weeks of the training. As for the early improvement of balance, one potential reason may be that fast strength gain occurs in muscles, during the first weeks of training, due to the neural adaptation and muscle fiber recruitment [17, 21, 39, 43]. Nonetheless, the neural adaptation appears as a transient response, during the first two weeks of training [21], which is shown to have transient central manifestation as well [11]. Apparently, after two weeks of training, the neural changes grow to physiological changes and muscular hypertrophy [44, 45]; which in turn translates to enough strength to significantly influence postural stability at week four. It is well evidenced that enough muscular strength directly contributes to postural stability [9, 39, 46]. The developed stability over a short time span of four weeks, is also in agreement with other studies which noticed improvements in balance performance (such as Berg balance scale, sensory organization test, limit of stability) by minimum of four weeks of training [23, 43, 47]. Furthermore, results revealed that the proposed model-based measures are more conservative than the postural sway measures, considering the smaller value of significance for KP (or Kn) as compared to f95 and ∆tc (or MV). This is because model-based measures are expressing some more subtle underlying neurophysiology of postural control.
The plateaued behavior in stability-related measures after some early rise was observed in some previous studies. Corcos et al. [41] noted such plateaued behavior in mean elbow flexion torque after 6 months, in favor of the PRE group compared to non-progressive control group which was even worsened over the two-year training program. This is while both PRE and control group had shown similar strength gain during the first 6 months of training; indicating that strength gain is achievable to some extent, regardless of the training program. However, regarding the chronic feature of PD [8, 21], further strengthening demands more focused progressive programs. This observation supports the impression that the attainable strength, and as such the learning capacity for postural stability in PD patients may be limited and has tendency to stop after a while. Likewise, Peterson et al. [28] claimed that people with PD may exhibit early, but not continued improvement in balance performance by training. In their study, the postural responses to translational perturbations in one-day practice were investigated in PD and healthy controls. Unlike healthy controls, improvements in people with PD occurred primarily in the first blocks of trials and then plateaued; whereas healthy controls gradually improved over all blocks of trials [28]. Other possible explanations for such behavior may be the insufficiency of the challenges and stimulus provided in the exercises, or the induced fatigue and detraining effects during the two closing weeks of the program [14, 39, 48]. However, it is less probable in our study since we employed a progressive difficulty level for the exercises throughout sessions. Interestingly, unlike RMS and f95, which plateaued at a steady level, KP and ∆tc-FO relatively reverted back to baseline. There are also studies that addressed such regress-to-baseline pattern in postural sway measures during a training program [48, 49]. However, these results should be interpreted cautiously, given the inherent bounds, or the maximum/minimum normal value that any measure such as KP, f95, etc. can attain and may stagnate at that level.
As an intriguing finding, our results revealed that improvements in some measures (e.g. MV, Kn, ∆tc, f95) occurred sooner (or with stronger significant difference) in EO condition than the EC condition, likely because EC tasks are more difficult. From this perspective, the continuous improvement in Tandem-EC and ∆tc-FC, compared to the saturated improvement in Tandem-EO and ∆tc-FO is explained. Similarly, τd showed decline only in EO tasks (RO and FO).
This study had limitations. The inclusion of a PD control group as well as a healthy control group as to limit the placebo effects is lacking. Furthermore, it is intriguing for future studies to design longer interventions with more assessment times during the intervention, as well as during the follow-up inspection. As such, future studies can discover an analytical formula for learning dynamics and dose-response relationships of postural control. Using longer training programs may also reveal the change patterns for other measures such as KI and KD, which was non-significant in the current study. Future studies also can employ targeted exercises to define the exact added value of each modality.