Susanne M. Morton

Cerebellar Contributions to Locomotor Adaptations during Splitbelt Treadmill Walking

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.

Cerebellar Control of Balance and Locomotion

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.

Mechanisms of cerebellar gait ataxia

The cerebellum is important for movement control and plays a critical role in balance and locomotion. As such, one of the most characteristic and sensitive signs of cerebellar damage is gait ataxia. How the cerebellum normally contributes to locomotor behavior is unknown, though recent work suggests that it helps generate appropriate patterns of limb movements, dynamically regulate upright posture and balance, and adjust the feedforward control of locomotor output through errorfeedback learning. The purpose of this review is to examine mechanisms of cerebellar control of locomotion, emphasizing studies of humans and other animals. Implications for rehabilitation are also considered.

Neurophysiologic and Rehabilitation Insights From the Split-Belt and Other Locomotor Adaptation Paradigms

Locomotion is incredibly flexible. Humans are able to stay upright and navigate long distances in the face of ever-changing environments and varied task demands, such as walking while carrying a heavy object or in thick mud. The focus of this review is a behavior that is critical for this flexibility: motor adaptation. Adaptation is defined here as the process of adjusting a movement to new demands through trial-and-error practice. A key feature of adaptation is that more practice without the new demand is required to return the movement to its original state. Thus, motor adaptation is a short-term motor learning process. Several studies have been undertaken to determine how humans adapt walking to novel circumstances. Many of these studies have examined locomotor adaptation using a split-belt treadmill. The results of these studies of people who were healthy and people with neurologic damage suggest that the cerebellum is required for normal adaptation of walking and that the role of cerebral structures may be less critical. They also suggest that intersegmental and interlimb coordination is critical but readily adaptable to accommodate changes in the environment. Locomotor adaptation also can be used to determine the walking potential of people with specific neurologic deficits. For instance, split-belt and limb-weighting locomotor adaptation studies show that adults with chronic stroke are capable of improving weight-bearing and spatiotemporal symmetry, at least temporarily. Our challenge as rehabilitation specialists is to intervene in ways that maximize this capacity.

Younger is not always better: development of locomotor adaptation from childhood to adulthood.

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.

Mechanisms of Short-Term Training-Induced Reaching Improvement in Severely Hemiparetic Stroke Patients: A TMS Study

Background. The neurophysiological mechanisms underlying improved upper-extremity motor skills have been partially investigated in patients with good motor recovery but are poorly understood in more impaired individuals, the majority of stroke survivors. Objective. The authors studied changes in primary motor cortex (M1) excitability (motor evoked potentials [MEPs], contralateral and ipsilateral silent periods [CSPs and ISPs] using transcranial magnetic stimulation [TMS]) associated with training-induced reaching improvement in stroke patients with severe arm paresis (n = 11; Upper-Extremity Fugl-Meyer score (F-M) = 27 ± 6). Methods. All patients underwent a single session of reaching training focused on moving the affected hand from a resting site to a target placed at 80% of maximum forward reaching amplitude in response to a visual “GO” cue. Triceps contribute primarily as agonist and biceps primarily as antagonist to the trained forward reaching movement. Response times were recorded for each reaching movement. Results. Preceding training (baseline), greater interhemispheric inhibition (measured by ISP) in the affected triceps muscle, reflecting inhibition from the nonlesioned to the lesioned M1, was observed in patients with lower F-M scores (more severe motor impairment). Training-induced improvements in reaching were greater in patients with slower response times at baseline. Increased MEP amplitudes and decreased ISPs and CSPs were observed in the affected triceps but not in the biceps muscle after training. Conclusion. These results indicate that along with training-induced motor improvements, training-specific modulation of intrahemispheric and interhemispheric mechanisms occurs after reaching practice in chronic stroke patients with substantial arm impairment.

Impaired Reactive Stepping Adjustments in Older Adults

Background The ability to redirect the path of the foot during walking is critical for responding to perturbations and maintaining upright stability. The purpose of the current study was to compare mechanisms of reactive stepping adjustments in young versus older adults when responding to an unexpected perturbation during voluntary step initiation. Methods We tested 13 healthy community-dwelling older adults and an equal number of young control participants performing stepping movements onto a visual target on the floor. In some trials, perturbations were introduced by unexpectedly shifting the target, at various time points, from its usual location to a new location 20 cm to the right. We measured ground reaction forces under the supporting leg and three-dimensional kinematics of the stepping leg in baseline and target shift trials. Results During target shift trials, that is, when reactive adjustments were required, older adults demonstrated the following: delayed responses in modifying the lateral propulsive forces under the supporting foot, reduced rates of lateral force production, delayed responses in modifying the stepping foot trajectory, and prolonged movement execution times. Conclusions The current study quantitatively distinguishes between healthy older and young adults in generating reactive stepping adjustments to an unpredictable shift of a visual target. The decreased capability for rapidly planning and executing an effective voluntary step modification could reveal one potential cause for the increased risk of falls in the older population.

Bilateral adaptation during locomotion following a unilaterally applied resistance to swing in nondisabled adults.

Human walking must be flexible enough to accommodate many contexts and goals. One form of this flexibility is locomotor adaptation: a practice-dependent alteration to walking occurring in response to some novel perturbing stimulus. Although studies have examined locomotor adaptation and its storage by the CNS in humans, it remains unclear whether altered movements occurring in the leg contralateral to a perturbation are caused by true practice-dependent adaptation or whether they are generated via feedback corrective mechanisms. To test this, we recorded leg kinematics and electromyography (EMG) from nondisabled adults as they walked on a treadmill before, during, and after a novel force was applied to one leg, which resisted its forward movement during swing phase. The perturbation produced kinematic changes to numerous walking parameters, including swing phase durations, step lengths, and hip angular excursions. Nearly all occurred bilaterally. Importantly, kinematic changes were gradually adjusted over a period of exposure to the perturbation and were associated with negative aftereffects on its removal, suggesting they were adjusted through a true motor adaptation process. In addition, increases in the EMG of both legs persisted even after the perturbation was removed, providing further evidence that the CNS made and stored changes to feedforward motor commands controlling each leg. Our results show evidence for a feedforward adaptation of walking involving the leg opposite a perturbation. This result may help support the application of locomotor adaptation paradigms in clinical rehabilitation interventions targeting recovery of symmetric walking patterns in a variety of patient populations.

Poststroke hemiparesis impairs the rate but not magnitude of adaptation of spatial and temporal locomotor features.

Background. Persons with stroke and hemiparesis walk with a characteristic pattern of spatial and temporal asymmetry that is resistant to most traditional interventions. It was recently shown in nondisabled persons that the degree of walking symmetry can be readily altered via locomotor adaptation. However, it is unclear whether stroke-related brain damage affects the ability to adapt spatial or temporal gait symmetry. Objective. Determine whether locomotor adaptation to a novel swing phase perturbation is impaired in persons with chronic stroke and hemiparesis. Methods. Participants with ischemic stroke (14) and nondisabled controls (12) walked on a treadmill before, during, and after adaptation to a unilateral perturbing weight that resisted forward leg movement. Leg kinematics were measured bilaterally, including step length and single-limb support (SLS) time symmetry, limb angle center of oscillation, and interlimb phasing, and magnitude of “initial” and “late” locomotor adaptation rates were determined. Results. All participants had similar magnitudes of adaptation and similar initial adaptation rates both spatially and temporally. All 14 participants with stroke and baseline asymmetry temporarily walked with improved SLS time symmetry after adaptation. However, late adaptation rates poststroke were decreased (took more strides to achieve adaptation) compared with controls. Conclusions. Mild to moderate hemiparesis does not interfere with the initial acquisition of novel symmetrical gait patterns in both the spatial and temporal domains, though it does disrupt the rate at which “late” adaptive changes are produced. Impairment of the late, slow phase of learning may be an important rehabilitation consideration in this patient population.

Cerebellar damage produces context-dependent deficits in control of leg dynamics during obstacle avoidance

It has been suggested that the cerebellum is an important contributor to CNS prediction and control of intersegmental dynamics during voluntary multijoint reaching movements. Leg movements subserve different behavioral goals, e.g., locomotion versus voluntary stepping, which may or may not be under similar dynamic control. The objective was to determine whether cerebellar leg hypermetria (excessive foot elevation) during obstacle avoidance in locomotion and voluntary stepping could be attributed to a particular deficit in appropriately controlling intersegmental dynamics. We compared the performance of eight individuals with cerebellar damage to eight healthy controls as they walked or voluntarily stepped in place over a small obstacle. Joint kinematics and dynamics were calculated during swing phase for both movement contexts. The kinematic analysis showed that hypermetria occurred during both walking and stepping and was associated with excessive knee flexion. When present, the amplitude of hypermetria was greater during stepping compared to walking. During stepping, subjects with cerebellar damage produced excessive knee flexor muscle torques and consequently overcompensated for interaction and gravitational torques normally used to decelerate the limb. During walking, the torque pattern was very similar to that of control subjects walking over a taller obstacle, and therefore might be a voluntary compensatory strategy to avoid tripping. Our results show that the extent of kinematic and dynamic abnormalities associated with cerebellar leg hypermetria is context-specific, with more fundamental abnormalities of leg dynamics being apparent during stepping as opposed to walking.