Responses following LL-NP/L outward perturbations
Kinematics and kinetics
Figure 2 shows COP, COM, and GRF responses under the experimental conditions before training (BEFORE_60 – left column) and after training (AFTER_60 and AFTER_90 – middle column) compared to those of the control (CONTROL_60 and CONTROL_90 – right column).
Prior to the training (BEFORE_60), the individual post-stroke responded with an in-stance strategy on the non-paretic left leg (NP/L) by substantially shifting COPx laterally in the direction of the perturbation (0–25% of gait cycle – GC; Fig. 2, 2nd row); this was done partially through using an ankle strategy and partially by repositioning the stance foot by rapidly moving COPy (0–25% of gait cycle – GC; Fig. 2, 4th row) first toward the toes, to enable the heel to lift slightly and move laterally by pivoting the stance leg around the toes, followed by rapid displacement of COPy toward the heel to enable lifting slightly the forefoot, bringing it also laterally by pivoting the stance leg around the heel. In addition, a noticeable GRFx (Fig. 2, 3rd row) force impulse was generated under the non-paretic left leg (0–25% of GC) using the hip strategy. The in-stance response described fully arrested the movement of COMx (Fig. 2, 2nd row) initiated by the perturbation at about 25% of GC. However, the described displacements of COPy during the period from 0 to 50% of GC also provoked a substantial alternating movement of COMy (Fig. 2, 4th row) first backward (0–50% of GC) and later (100–150% of GC) forward. The in-stance postural response described was sufficient to efficiently counteract the perturbation and was similar to the control response (CONTROL_60) except for the in-stance repositioning of the foot.
After the training (AFTER_60), the individual post-stroke abandoned the strategy of repositioning the stance foot – once planted on the ground, the non-paretic left leg remained in the same location and orientation. This is confirmed by the shapes of COPy and GRFy (0 to 25% of GC, Fig. 2, 4th and 5th row) which are shape-wise similar to unperturbed walking and no longer display the oscillatory behavior noted prior to the training (BEFORE_60). Once again an in-stance strategy (0–50% of GC) composed of displacement of COPx (Fig. 2, 2nd row) laterally together with generation of a GRFx impulse (0–25% of GC; Fig. 2, 3rd row) on the non-paretic stance leg (NP/L0) was utilized. However, after the training, the stepping strategy was also partially utilized, as can be seen from the displacement of COPx (50–100% of GC), which differs noticeably from that in the unperturbed condition. The displacement of COMy backward (0–50% of GC) and then forward (100–150% of GC) was still present after training.
At the higher amplitude of perturbation (AFTER_90), the in-stance strategy alone was not sufficient. Apart from the ankle and hip in-stance strategies described, the first two steps use a stepping strategy, first with the right leg (P/R1) followed by the left leg (NP/L1) (50–150% of GC), which can be observed from COPx (50–150% of GC; Fig. 2, 3rd row). In the frontal plane, this postural response is very similar to the control response (CONTROL_90). In the sagittal plane, the responses are similar in the early phase (0–100%) but the individual post-stroke demonstrated a significant forward excursion of COMy (Fig. 2, 4th row) in the late phase (100–150%).
Spatio-temporal parameters
Figure 3 displays mean values and standard deviations for step lengths, widths, and times in all experimental conditions.
Step lengths were similar in the BEFORE_60, AFTER_60 and CONTROL_60 experimental conditions. There was a noticeable difference in step widths for the first two steps after the perturbation (P/R1 and NP/L1): substantially smaller step widths were recorded in the AFTER_60 condition than in the BEFORE_60 and CONTROL_60 conditions. It is evident from the temporal parameters for the BEFORE_60 and AFTER_60 experimental conditions that the step time of the first right step with the paretic leg (P/R) following the perturbation (P/R1) was much longer, facilitating the in-stance response on the left leg (NP/L0) described, which was similar to the control response (CONTROL_60). The second step of the left leg (NP/L1) that followed was substantially faster than the control response (CONTROL_60).
Comparison of experimental conditions AFTER_90 and CONTROL_90 shows a substantially longer first step (P/R1) for the individual post-stroke. The step widths and step times for the first step (P/R1) were similar, indicating the marked stepping response.
Electromyography
Figure 4 shows EMG responses of the lower limb muscles in both legs under all experimental conditions. A qualitative comparison of the muscular activity of the non-paretic left leg of the individual post-stroke and the left leg of the control participant shows substantial similarity in the action of all muscles throughout the response across all experimental conditions. In all experimental conditions, there is a marked increase of activity in all muscles from 0 to 50% of GC during perturbed walking when compared to unperturbed walking and this reflects the in-stance responses. There are however distinct differences predominantly in the SOL, GM, GL, RF and GMAX muscles of the non-paretic leg in the period from 0 to 50% of GC where oscillations related to re-positioning of the foot by pivoting first around the toes followed by pivoting around the heel can be clearly observed in the experimental condition BEFORE_60 while after the training this oscillatory behavior is no longer present in the experimental conditions AFTER_60 and AFTER_90. From 50 to 250% of GC, the muscular activity during perturbed and unperturbed walking is substantially similar. When comparing the muscular activity of the paretic leg of the individual post-stroke and the right leg of the control participant, a marked increase of activity in RF and TA from 0 to 50% of GC can be seen for all experimental conditions and a co-contraction of ST can be also observed in the individual post-stroke.
Responses following RR-P/R outward perturbations
Kinematics and kinetics
Figure 5 shows COP, COM, and GRF responses under the experimental conditions before training (BEFORE_60 – left column), after training (AFTER_60 and AFTER_90 – middle column) compared to those of the control (CONTROL_60 and CONTROL_90 – right column).
Prior to the training (BEFORE_60), an in-stance response is almost completely absent for the entire stance phase of the right-paretic leg. COPx after the perturbation (0–50% of GC; Fig. 5, 2nd row) is similar to that during unperturbed walking, indicating that an ankle strategy was not used, and the GRFx (Fig. 5, 3rd row) force impulse seen during the first 25% of the stance in response to a LL-NP/L perturbation is absent, indicating that a hip strategy is not used either. Therefore, throughout the entire stance phase of the impaired leg (0–50% of GC), COMx (Fig. 5, 2nd row) is almost freely displaced in the direction of the perturbation. Only after the non-paretic left leg (NP/L1) enters the stance (50–100% of GC) by making a cross-step – which can be seen from the substantial displacement of COPx (50–100% of GC) to the right when compared to unperturbed walking – is movement of COMx decelerated and then fully arrested by the next step of the paretic right leg when COPx is displaced even more to the right (P/R1; 100–150% of GC). The complete absence of in-stance response during P/R0 stance (0–50% of GC) also has implications for the movement of COMy (Fig. 5, 4th row). Throughout the first step with the left leg (NP/L1) following the perturbation, there is a pronounced rise in GRFy (50–100% of GC; Fig. 5, 5th row) compared to that seen during unperturbed walking and COMy (Fig. 5, 4th row) is thus accelerating forward. This self-induced forward perturbation was handled in the next step with the right leg (P/R1) by displacing COPy substantially forward (100–150% of GC) thus increasing GRFy (100–150% of GC; Fig. 5, 5th row) in the backward direction to decelerate COMy. This balancing strategy is very different to the control response (CONTROL_60) which was, to a large extent, a mirror image of the response to LL-NP/L perturbation.
After the training (AFTER_60), the response remained qualitatively and functionally similar to that described above; however, there is a modest in-stance impulse in GRFx (0–50% of GC; Fig. 5, 3nr row) followed by a bigger GRFx impulse in the second right leg (P/R1) stance phase (50–150% of GC), as indicated in Fig. 6.
At the higher amplitude of perturbation (AFTER_90), the response was similar to the one at smaller amplitude of perturbation (AFTER_60); however, the first step of the left leg was even more lateral as can be seen from COPx (NP/L1; 50–100% of GC; Fig. 5, 2nd row) due to the larger displacement of COMx produced by the stronger perturbation.
Spatio-temporal parameters
Figure 7 displays mean values and standard deviations for step lengths, widths, and times in all experimental conditions.
Step lengths were similar in the BEFORE_60 and AFTER_60 experimental conditions, and differed markedly from the CONTROL_60 results, mainly in the first and the third steps after the perturbation. There was also a noticeable difference in step width for the first and third steps after the perturbation (NP/L1 and NP/L2): BEFORE_60 and AFTER_60 show a substantially smaller width for the first step and substantially bigger width for the third step than was seen in the CONTROL_60 experimental condition. It is evident from the temporal parameters for both the BEFORE_60 and AFTER_60 experimental conditions that the step time for the first step with the non-paretic left leg (NP/L1) following the perturbation was much shorter in the individual post-stroke. This enabled faster lateral displacement of the foot, and thus COPx, in the absence of an in-stance response.
A comparison of AFTER_90 and CONTROL_90 shows similar step lengths in each experimental condition but marked differences in step widths: the widths of the first steps (NP/L1) are similar but those of the next two steps (P/R1 and NP/L2) are substantially bigger for the individual post-stroke. Also the step time for the first step (NP/L1) after the perturbation is substantially shorter for the individual post-stroke and is similar to that seen in the experimental conditions BEFORE_60 and AFTER_60.
Electromyography
Figure 8 shows EMG responses of lower limb muscles in both legs under all experimental conditions. A qualitative comparison of the muscular activity of the paretic leg of the individual post-stroke during unperturbed walking and perturbed walking shows substantially similar activation in all experimental conditions (BEFORE_60, AFTER_60 and AFTER_90) indicating an almost complete lack of the in-stance response displayed by the control participant through increased activation of all the muscles of the right leg, predominantly in the period from 0 to 50% of GC (experimental conditions CONTROL_60 and CONTROL_90). A qualitative comparison of the muscular activity of the non-paretic leg of the individual post-stroke and the left leg of the control participant showed there was substantially similar activation of all muscles in all experimental conditions.
Clinical outcome measures
Table 1 shows the performance of the individual post-stroke before and after the thirty training sessions and demonstrates improvement in all the assessed clinical outcome measures.
Table 1 Clinical outcome measures assessed in the post-stroke subject before and after the 30 training sessions