Implications of assist-as-needed robotic step training after a complete spinal cord injury on intrinsic strategies of motor learning

Abstract

Robotic training paradigms that enforce a fixed kinematic control might be suboptimal for rehabilitative training because they abolish variability, an intrinsic property of neuromuscular control (Jezernik et al., 2003). In the present study we introduce "assist-as-needed" (AAN) robotic training paradigms for rehabilitation of spinal cord injury subjects. To test the efficacy of these robotic control strategies to teach spinal mice to step, we divided 27 adult female Swiss-Webster mice randomly into three groups. Each group was trained robotically by using one of three control strategies: a fixed training trajectory (Fixed group), an AAN training paradigm without interlimb coordination (Band group), and an AAN training paradigm with bilateral hindlimb coordination (Window group). Beginning at 14 d after a complete midthoracic spinal cord transection, the mice were trained daily (10 min/d, 5 d/week) to step on a treadmill 10 min after the administration of quipazine (0.5 mg/kg), a serotonin agonist, for a period of 6 weeks. During weekly performance evaluations, the mice trained with the AAN window paradigm generally showed the highest level of recovery as measured by the number, consistency, and periodicity of steps during the testing sessions. In all three measurements there were no significant differences between the Band and the Fixed training groups. These results indicate that the window training approach, which includes loose alternating interlimb coordination, is more effective than a fixed trajectory paradigm with rigid alternating interlimb coordination or an AAN paradigm without any interlimb constraints in promoting robust postinjury stepping behavior.

Figure 1.

a, AAN training paradigm I (Band). The solid thick line shows the desired training trajectory of the animal's ankle position in the sagittal plane. The dashed thin lines represent the boundaries within which “soft control” (see Materials and Methods) is applied to the limbs. The arrows outside the boundaries correspond to the convergent velocity fields that drive the legs to the band region. Modified from Cai et al. (2005). b, AAN training paradigm II (Window). The solid line represents the desired training trajectory of the animal's ankle position in the sagittal plane, and the moving window is outlined by the dotted circle within which soft control is applied to the limbs. The arrows outside the circle correspond to the radial force fields. Modified from Cai et al. (2005).

Figure 2.

The stepping trajectories of the ankle of a neonatally spinal cord transected mouse at ∼3 months of age. The diagonal line through the trajectories shows where the most deviation (∼4 mm) occurs. The arrows represent the direction of travel.

Figure 3.

Locomotor performance of the best 12 s interval by each of the three groups during the weekly tests as measured by (a) average number of steps performed, (b) step rhythmicity as depicted by the plot of the inverse FWHM, and (c) step shape consistency as measured by PCA. On average, the Window group performed better when compared with the other two groups. +, Denotes significant difference between the Window and the Fixed groups; #, denotes significant difference between the Window and Band groups.