Locomotor adaptability ranges from the simple and fast-acting to the complex and long-lasting and is a requirement for successful mobility in an unpredictable environment. Several neural structures, including the spinal cord, brainstem, cerebellum, and motor cortex, have been implicated in the control of various types of locomotor adaptation. However, it is not known which structures control which types of adaptation and the specific mechanisms by which the appropriate adjustments are made. Here, we used a splitbelt treadmill to test cerebellar contributions to two different forms of locomotor adaptation in humans. We found that cerebellar damage does not impair the ability to make reactive feedback-driven motor adaptations, but significantly disrupts predictive feedforward motor adaptations during splitbelt treadmill locomotion. Our results speak to two important aspects of locomotor control. First, we have demonstrated that different levels of locomotor adaptability are clearly dissociable. Second, the cerebellum seems to play an essential role in predictive but not reactive locomotor adjustments. We postulate that reactive adjustments may instead be predominantly controlled by lower neural centers, such as the spinal cord or brainstem.

The cerebellum is important for movement control and plays a particularly crucial role in balance and locomotion. As such, one of the most characteristic signs of cerebellar damage is walking ataxia. It is not known how the cerebellum normally contributes to walking, although recent work suggests that it plays a role in the generation of appropriate patterns of limb movements, dynamic regulation of balance, and adaptation of posture and locomotion through practice. The purpose of this review is to examine mechanisms of cerebellar control of balance and locomotion, emphasizing studies of humans and other animals. Implications for rehabilitation are also considered.

New walking patterns can be learned over short timescales (i.e., adapted in minutes) using a split-belt treadmill that controls the speed of each leg independently. This leads to storage of a modified spatial and temporal motor pattern that is expressed as an aftereffect in regular walking conditions. Because split-belt walking is a novel task for adults and children alike, we used it to investigate how motor adaptation matures during human development. We also asked whether the immature pattern resembles that of people with cerebellar dysfunction, because we know that this adaptation depends on cerebellar integrity. Healthy children (3-18 years old) and adults, and individuals with cerebellar damage were adapted while walking on split belts (1:2 speed ratio). Adaptation and de-adaptation rates were quantified separately for temporal and spatial parameters. All healthy children and adults tested could learn the new timing at the same rate and showed significant aftereffects. However, children younger than 6 years old were unable to learn the new spatial coordination. Furthermore, children as old as age 11 years old showed slower rates of adaptation and de-adaptation of spatial parameters of walking. Young children showed patterns similar to cerebellar patients, with greater deficits in spatial versus temporal adaptation. Thus, although walking is a well-practiced, refined motor skill by late childhood (i.e., 11 years of age), the processes underlying learning new spatial relationships between the legs are still developing. The maturation of locomotor adaptation follows at least two time courses, which we propose is determined by the developmental state of the cerebellum.

Adaptation of arm movements to laterally displacing prism glasses is usually highly specific to body part and movement type and is known to require the cerebellum. Here, we show that prism adaptation of walking trajectory generalizes to reaching (a different behavior involving a different body part) and that this adaptation requires the cerebellum. In experiment 1, healthy control subjects adapted to prisms during either reaching or walking and were tested for generalization to the other movement type. We recorded lateral deviations in finger endpoint position and walking direction to measure negative aftereffects and generalization. Results showed that generalization of prism adaptation is asymmetric: walking generalizes extensively to reaching, but reaching does not generalize to walking. In experiment 2, we compared the performance of cerebellar subjects versus healthy controls during the prism walking adaptation. We measured rates of adaptation, aftereffects, and generalization. Cerebellar subjects had reduced adaptation magnitudes, slowed adaptation rates, decreased negative aftereffects, and poor generalization. Based on these experiments, we propose that prism adaptation during whole body movements through space invokes a more general system for visuomotor remapping, involving recalibration of higher-order, effector-independent brain regions. In contrast, prism adaptation during isolated movements of the limbs is probably recalibrated by effector-specific mechanisms. The cerebellum is an essential component in the network for both types of prism adaptation.