Residual deficits contribute to a new walking strategy after mild SCI
Using the BBB scale, spontaneous recovery occurred over 21 days after mild SCI but residual impairments prevented normal locomotion (). Mild SCI resulted in severe paresis with slight and extensive HL movements 1 day after SCI (Mean BBB = 6.83 ± 0.655). Weight supported stepping recovered within 7 days. Despite rapid improvement, recovery plateaued at levels significantly below normal at 21 days (Mean BBB = 15.75 ± 1.085; P < 0.05). While one animal attained near normal locomotion (BBB = 19), remaining animals had persistent trunk instability (100%), toe dragging (37.5%), and paw rotation at lift off (100%) or initial contact (37.5%).
Figure 1 Open field locomotion. Spontaneous recovery occurred in the open field after mild SCI. BBB scores plateaued by 21 days and remained significantly lower than control (mean SCI = 15.7 ± 1.085). Residual deficits at 21 days included toe dragging, (more ...)
Using 2D TM kinematics, we quantified the plateaued walking behavior across subphases of locomotion (; Basso et al. 1994
). Hip movements are biphasic and include two subphases, flexion (F) and extension (E). Knee and ankle movements are more complex and are divided into four subphases (E1, E2, E3, F). The first extension subphase (E1) occurs from peak flexion in swing until initial paw contact on the ground. The E2 subphase, from initial contact through weight acceptance, represents joint flexion during yield and relies on eccentric muscle lengthening. During E3, midstance to lift off, all joints extend. Lift off to peak flexion represents the flexion (F) subphase. Thus, stance includes E2 and E3 and swing includes F and E1 ().
Figure 2 Stick figure diagrams at the end of each phase of gait illustrate prolonged extension during TM locomotion. Subphases of locomotion include E1, E2, E3, and F. The third extension phase (E3) occurs from midstance to lift off where knee and ankle extension (more ...)
After recovery from SCI, the position of the paw relative to the pelvis showed significant caudal displacement during all phases of gait (). The caudal shift for injured rats (dotted lines) was 2.39 ± 0.23 cm (P < 0.01) at lift off and 1.24 ± 0.29 cm (P < 0.01) at initial contact compared to naive (solid lines; ). During E1, a 43% reduction in forward swing occurred after SCI (3.35 ± 0.473 cm, SCI; 5.88 ± 0.488 cm, Naive; P < 0.05). This caudal shift was reflected in significant differences in angular excursion of all HL joints (). Knee and ankle extension decreased during late swing (E1) and yield (E2) (P < 0.05). Significantly greater extension occurred in the hip, knee, and ankle during late stance (E3), leading to more excursion during flexion (F) after SCI (P < 0.05). The increase in flexion was not due to hypermetria as toe height was reduced after injury (toe height: 1.88 ± 0.151 cm, SCI; 2.10 ± 0.174 cm, Naive; ); rather, greater flexion represented the return from prolonged extension at lift off. At lift off, the pelvis was on average 0.78 cm higher after SCI in 60% of animals. Implantation of EMG electrodes did not affect joint angular excursion (compare Naive and LAM groups, ).
Figure 3 Angular excursion profiles of hip, knee, and ankle joints. Precise kinematic analysis of joint excursion between different phases of gait reveal altered biomechanics after SCI. Extension of the knee and ankle significantly increased from late stance to (more ...)
Recovery of intralimb coordination occurs in a proximal to distal manner
To examine coordinated movement between HL joints during locomotion, angle–angle diagrams were constructed by plotting the excursion of one joint against another. Coordination between proximal (hip–knee) or distal (knee–ankle) joints was compared to determine the extent of recovery. Angle–angle diagrams display joint excursion, position of the joints during excursion, and the coordination between joints (Basso et al. 1994
). In normal locomotion, a curvilinear shape emerges when one joint moves to a greater extent (more excursion) than the other joint (). Fine motor control is made evident by fractionated movement, or independent control of joints. Fractionation is most clearly demonstrated in E2, where HL joints are required to flex while another extends. Intralimb coordination results when a reproducible and precise curvilinear pattern of movement occurs over multiple step cycles.
Figure 4 Fractionated movement in proximal and distal joints. Angle–angle plots were used to describe intralimb coordination between proximal (hip–knee) or distal (knee–ankle) joints. Naive plots depict curvilinear patterns between the (more ...)
After recovery from SCI, coordination between distal (knee and ankle) joints is most impaired. Linear rather than curvilinear paths depict poor fractionated joint movements. The linear pattern during stance results from a lack of E2 or yield phase (). The knee and ankle had equivalent changes in excursion and did not flex or extend in opposition to each other. Proximal coordination between the hip and knee was less impaired but a change in shape and position of the angle–angle plot was apparent (). A second flexion occurred at the knee during E2 (arrow, ). A double yield was observed in 55% of animals. Prolonged extension is evident by the rightward and upward shift in position of the post op hip–knee and knee–ankle plots. At E3, the hip becomes approximately two times more extended than the knee, demonstrating greater proximal extension ().
Joint kinematics and timing of muscle activity
In naive animals, TA onset occurs with ankle dorsiflexion while LG onset occurs with plantar flexion before ground contact (). Both muscles are briefly coactive during terminal swing. TA offset occurs prior to plantar flexion and E1 (mean duration = 210.8 msec), and LG remains active during stance (mean duration = 442.9 msec). The dual-burst pattern of ST coincides with extension and flexion in the hip and knee. Onset of ST1 occurs during hip extension (mean duration = 156.8 msec) and ST2 during knee flexion through weight acceptance (mean duration = 248.2 msec). The double burst is separated by a brief pause during E1 while the hip flexes and the knee extends in midswing to move the paw forward.
Figure 5 Comparison of HL muscle activity with changes in angular kinematics before and after SCI. EMG activity is aligned with kinematics of the hip, knee, and ankle in the same animal before and 21 days after mild SCI. The vertical line marks stance onset. Black (more ...)
Timing and overall pattern of muscle recruitment changed after injury alongside altered joint kinematics. At the ankle, marked changes were evident compared to naive that were maintained throughout recovery. At 21 days, plantar flexion is absent at the ankle and LG onset instead occurs during a period of prolonged dorsiflexion before ground contact (). A reduction in burst duration is apparent in both muscles relative to naive-TA (–25.6 ± 7.5%); LG (–44.1 ± 12.0%). These reductions were independent of recovery in the open field ().
Figure 6 Activation patterns of the semitendinosis change with recovery. EMG activity is plotted in the same animal over time. The vertical line marks stance onset. Seven days after SCI, forelimb–hindlimb coordination and plantar stepping was not consistent (more ...)
Activity of ST changed over time but did not return to normal by 21 days. Early after SCI, with only frequent stepping and limited forelimb–hindlimb coordination (BBB = 12) at 7 days, the dual-burst pattern of the ST is lost and only a single prolonged burst occurs. Dual bursts return by 21 days when coordination and stepping frequency recover (BBB = 15; ). ST1 fires later throughout recovery and occurs ~101.9 msec closer to initial contact, and for shorter duration (–11.3 ± 24.5%) compared to naive (). After recovery, ST2 activation is delayed (35.9 msec) and fires at higher amplitude compared to 7 days. There is notable variability in ST2 firing patterns, as ST2 duration was on average +33.6 ± 46.13% longer at 21 days (). In low (BBB = 16), but not high performing animals, ST2 activation occurs with knee flexion instead of extension during yield (). To determine whether differences in ST2 duration were linear with recovery, burst durations were normalized (percent change postinjury) and correlated with open field BBB scores. A high correlation between ST2 burst duration and BBB scores (r2 = 0.9697; P < 0.05) indicates that smaller changes in burst duration occur in high-performing animals ().
Figure 7 Average burst duration relative to stance onset. Burst durations were measured relative to stance onset (“0”) and averaged before (solid) and 21 days (hatched) after injury. Average EMG onset and offset times are marked by the beginning (more ...)
Figure 8 ST2 burst duration predicts recovery in the open field. Normalized burst durations were correlated with BBB scores ranging from 15 to 19. TA, LG, and ST1 display shortened burst durations relative to normal that do not correlate with open field performance (more ...)
Changes in ST reflect task specificity
To determine whether different forms of TM locomotion alter muscle recruitment after SCI, we compared flat or 10% downslope grade TM walking in the same animals. Similar to 7 days and 21 days, flat TM walking at 13 days showed delayed activation of ST1 and shorter-burst durations relative to normal. During flat walking, a single prolonged burst with an indiscriminate reset period occurs in ST and ST2 is negligible (). TM walking at a downslope grade required a different recruitment pattern that was identified by changes in the ST. Downslope walking produced later, and less activation of TA for ankle dorsiflexion and recruitment of LG was unchanged (data not shown). In the ST, downslope walking re-established a dual-burst pattern (). Notably, ST2 fired at a greater amplitude with a more defined onset/offset period during downslope walking than flat TM walking (). While downslope walking produced a reset period between ST1 and ST2 within the time period described for Naives, the muscle was not silent.
Figure 9 Task-specific changes in locomotion alter ST recruitment after mild SCI. EMG recordings are shown for the same animal as Naive, and 13 days after injury while walking on flat or 10% downhill TM surface grades. Stick figure diagrams at 60 Hz show a representative (more ...)