Intralimb coordination as a sensitive indicator of motor-control impairment after spinal cord injury

Abstract

Background: Recovery of walking function after neurotrauma, e.g., after spinal cord injury, is routinely captured using standardized walking outcome measures of time and distance. However, these measures do not provide information on possible underlying mechanisms of recovery, nor do they tell anything about the quality of gait. Subjects with an incomplete spinal cord injury are a very heterogeneous group of people with a wide range of functional impairments. A stratification of these subjects would allow increasing sensitivity for hypothesis testing and a more targeted treatment strategy.

Methods: The gait of incomplete spinal cord injured subjects was compared to healthy control subjects by analyzing kinematic data obtained by a 3-D motion capture system. Hip-knee angle-angle plots (cyclograms) informed on the qualitative aspect of gait and the intralimb coordination. Features of the cyclogram, e.g., shape of the cyclogram, cycle-to-cycle consistency and its modulation due to changes in walking speed were discerned and used to stratify spinal cord injured subjects.

Results: Spinal cord injured subjects were unable to modulate their cyclogram configuration when increasing speed from slow to preferred. Their gait quality remained clearly aberrant and showed even higher deviations from normal when walking at preferred speed. Qualitative categorization of spinal cord injured subjects based on their intralimb coordination was complemented by quantitative measures of cyclogram shape comparison.

Discussion: Spinal cord injured subjects showed distinct distortions of intralimb coordination as well as limited modulation to changes in walking speed. The specific changes of the cyclograms revealed complementary insight in the disturbance of lower-limb control in addition to measures of time and distance and may be a useful tool for patient categorization and stratification prior to clinical trial inclusion.

Keywords: categorization; coordination; cyclogram; gait; human; intralimb; spinal cord injury.

FIGURE 1

Hip-knee cyclograms of healthy controls and iSCI subjects. The hip–knee cyclogram of a healthy control subject with its typical characteristics is depicted in panel (A). iSCI subjects were classified into four groups of impairment, group 1 (unpredictable gait pattern) being the most affected group while group 4 (regular gait pattern) showed normal cyclograms (B). The criteria for each group are listed in the boxes on the left. The cyclograms in the left column show one representative example per group, the right column depicts the individual cyclograms of each iSCI subject within a group (dashed lines) and the group mean cyclogram (solid bold line) after translation of the cyclogram’s centroid to origin (zero) and uniform scaling.

FIGURE 2

(A) The cycle-to-cycle shape consistency within a subject is quantified as the angular component of coefficient of correspondence (ACC). This value can attain values between 0 (no congruency between cycles) and 1 (complete shape congruency from cycle to cycle). Both groups increased their cyclogram consistency when changing from a slow to preferred walking speed. iSCI subjects only showed lower values at preferred walking speed. Statistical significance (p < 0.0125) is indicated by an asterisk. Panel B shows the correlation indicated by Spearman’s ρ of the cyclogram ranking to preferred OG walking speed and to hip- and knee-ROMs (C). Little dots represent single values of individual subjects while the larger symbols represent the mean value per group.

FIGURE 3

Within-group cyclogram variability. The variability of the cyclogram between subjects within a group was quantified by the cumulated elliptic area for 20 bins per gait cycle (A). The half axes of the ellipse correspond to the between-subject standard deviation of the hip- and knee-angles, respectively. (B) shows the course of the variability at every time point of a gait cycle. The control group is represented by a black dashed line, iSCI group is depicted in red. The vertical lines mark the time point of toe-off.

FIGURE 4

The square root of the sum of squared distances (SSD) calculated the difference in shape of two figures. The cyclograms are shown after translation of the centroid to origin (zero) and uniform scaling. The control group is represented by a black dashed line, iSCI group is depicted in red. The straight black lines indicate the deviation of the two figures. a.u. = arbitrary units.