The following results refer to the PD subjects’ performance when they were “off” medication, except in the last section, which describes the effects of anti-parkinsonian medications. All subjects spontaneously exhibited FoG while moving about the laboratory prior to and following the protocol’s trials.
Large, rapid, backward translations of the support surface elicited three patterns of postural preparation (). The two most common patterns were (1) a single APA followed by a step () and (2) two to five (multiple) APAs followed by either a step or by a fall for PD subjects (). Much less frequently, subjects showed (3) no discernable APA preceding a step or fall (). The control subjects exhibited a fourth pattern: a single APA followed by a feet-in-place retention of balance in five out of 50 trials.
Relationships among APA response types, falls and FoG across groups
Fig. 2 Examples of APA response patterns during (A) protective step of a control subject, (B) protective step of a PD subject, (C) voluntary step for the same control subject, and (D) voluntary step of the same PD subject. The top graphs of each example illustrate (more ...)
Control subjects predominantly responded to the backward translation of the platform with a single APA, whereas the PD subjects responded with a single APA much less frequently (). The prevalence of trials with multiple APAs was significantly higher for the PD subjects than for the control subjects () [Mann-Whitney U = 2.94; P < 0.005]. The multiple APAs exhibited by the PD subjects were coincident with an alternating trembling of the knees that was apparent in the videos taken during the trials. Multiple APAs significantly delayed step onset in PD subjects [Kruskal Wallis χ2
= 18.44; P = 0.0001] (). The alternations of the vertical ground-reaction forces during multiple APAs occurred at a mean (± sd) frequency of 2.67 ± 0.95 Hz (illustrated in ). The trembling was not present before the movement of the platform and trembling was initiated by the platform translation at a latency that was consistent with the onset of the APAs (see video supplement
Fig. 3 Characteristics of the PD subject trials with multiple APAs. (A) Average APA amplitudes from the first, second, and third APA of a multiple-APA pattern. (B) Average APA onset latencies of the PD subjects’ multiple-APA trials compared to the control (more ...)
Seven of the 10 PD subjects exhibited FoG for an average (± 95% CI) prevalence of 34 ± 27% of trials based on our operational definition of FoG as trials with a step onset delayed beyond that of any control subject or no step followed by a fall. Trials with FoG generally occurred when multiple APAs were evident (). The PD subjects often rose up on their toes but were unable to lift the foot to take a step or the step was delayed. It was as though the toes were glued to the floor, as described by Yanagisawa et al.’s (1991)
definition of FoG. This phenomenon appeared identical to the FoG spontaneously exhibited by the PD subjects before and after the protocol testing when their center of mass was displaced forward.
The control subjects stepped on average (± 95% CI) in 84 ± 16% of the trials and regained balance without stepping in the other 16% of the trials. In contrast, the PD subjects stepped in 68 ± 24% of the trials. Failure to step was more commonly associated with multiple APAs. The PD subjects stepped in 57% of trials with multiple APAs compared to 82% of trials with one APA. The multiple APAs in control subjects consisted of only two APAs. The six multiple APA trials in control subjects were associated with a step in three trials and with a feet-in-place retention of balance in three trials.
No control subject fell with the forced step paradigm while six of the 10 PD subjects fell, for an average prevalence of 32 ± 28% of trials [Mann-Whitney U = 2.76; P < 0.02]. Eighty-eight percent of trials without a step coincided with a fall compared to 6% of trials with a step [χ2 = 33.31; P < 0.0001].
In contrast to what might have been predicted for a hypokinetic motor disorder, the peak amplitudes of the PD subjects’ first APA in a multiple-APA pattern tended to be larger than the single APAs of the control subjects: 27 ± 10% of body weight compared to 20 ± 8% of body weight, respectively [Mann Whitney U = 1.35; P = 0.18]. In addition, peak APA amplitudes became larger with repetition of APAs in the PD subjects who exhibited multiple APAs [Kruskal Wallis χ2 = 8.04; P < 0.05] (). Onset of the first APA in a multiple-APA pattern was not delayed for PD subjects, but occurred earlier than in the single-APA trials of the control subjects [Mann-Whitney U = 2.33; P < 0.05] (). Step onset latencies were also similar between the PD subjects who stepped and the control subjects when comparing across all response types [Mann-Whitney U = 0.61; P = 0.54]. The PD subjects’ step onset latencies, however, increased with multiple APAs [Kruskal Wallis χ2 = 18.44; P = 0.0001] ().
EMG Patterns to Initiate APAs Prior to Protective Stepping
The pattern of muscle activation responsible for APAs was similar for voluntary and protective step initiation, except that an additional medium-latency gastrocnemius burst was elicited as part of the automatic postural response to the surface translations prior to protective stepping. illustrates EMG activity during protective and voluntary stepping for a control subject and a PD subject.
Just as the APA onset latencies measured from forces were earlier for the PD subjects (), the EMG onset latencies of the tensor fascia latae, responsible for the lateral weight shift of the APA, were earlier for the PD subjects than the control subjects [for the swing limb: U = 2.00, P < 0.05; for the stance limb: U = 2.61, P < 0.01] (). In addition, the control subjects tended to activate the tensor fascia latae of the swing limb before that of the stance limb [Wilcoxon Signed Rank = 1.89; P = 0.06], whereas the PD subjects exhibited similar onset latencies (co-activation) across both limbs [Wilcoxon = 0.59; P = 0.55] (). The onset latency of the first tibialis anterior activation, responsible for the forward weight shift of the APA, was also earlier for the PD subjects than the control subjects [for the swing limb: U = 2.32, P < 0.05; for the stance limb: Mann-Whitney U = 2.29, P < 0.05] (). Multiple APAs were associated with reciprocal activation of right and left leg tibialis anterior (75% of multiple-APA trials), gastrocnemius (50% of multiple-APA trials), and tensor fascia latae (17% of multiple-APA trials) muscles.
EMG Onset Latencies to Platform Translations
Cued voluntary steps elicited similar step initiation patterns in the PD and control subjects, except that the PD subjects exhibited hypometric APAs () and delayed foot lift, as noted in our former study on voluntary stepping (Burleigh-Jacobs et al., 1997
). The mean (± 95% CI) APA amplitude was 18 ± 9% body weight for the PD subjects compared to 39 ± 9% body weight for the control subjects. The activation patterns of the tensor fascia latae and tibialis anterior muscles for generating APAs during voluntary step initiation were similar for the PD subjects and the control subjects. The tensor fascia latae and tibialis anterior muscles tended to activate prior to the onset of the first APA followed by activation of the gastrocnemius and then another tibialis anterior burst just prior to lifting the stepping foot (). With voluntary steps, multiple APAs with delayed step onsets were evident in a total of three trials from two PD subjects. The voluntary stepping trials never elicited clinically apparent FoG or falls in either subject group.
Effects of Antiparkinsonian Medications on Protective Steps
Antiparkinsonian medications decreased multiple APAs from 56 ± 23% of trials when “off” to 37 ± 21% of trials when “on” () The prevalence of FoG declined from 34 ± 27% of trials occurring in seven of 10 subjects when “off” to 20 ± 27% of trials occurring in three of nine subjects when “on.” Neither change reached significance by Wilcoxon Signed Rank tests. Falls, however, were reduced to a larger extent, from 32 ± 28% to 11 ± 21% and failure to step from 32 ± 28% to 15 ± 26% [both p = 0.06 by Wilcoxon Signed Rank test]. Thus the antiparkinsonian medications seemed to be more effective in reducing the consequences of multiple APAs and FoG, that is failure to step and falls, than in decreasing the events themselves.
The peak APA amplitudes, APA onset latencies, and the corresponding EMG onset latencies for the tensor fascia latae and the tibialis anterior were not significantly altered by medication. The lack of effect of levodopa on the peak amplitudes and latencies of the APAs associated with the protective steps is not surprising; as described above, peak amplitudes were normal and latencies were not prolonged. In contrast, levodopa augmented the APA amplitude in the voluntary stepping paradigm, as reported previously from our laboratory (Burleigh-Jacobs et al., 1997