Increasing Gait Automaticity in Older Adults by Exploiting Locomotor Adaptation

Restrictions in community mobility, the ability to move outside of one's home, are common in older ages and contribute to disability, institutionalization, and poor quality of life. Successful community mobility requires rapid integration of information from both external (e.g. surface quality, distances) and internal (e.g. fatigue, pain) to the individual. Under normal conditions, integration of these inputs occurs in subcortical-frontal (e.g., basal ganglia and cerebellum to primary motor cortex) networks and favors automatic motor control with few demands on the attention- related networks that primarily reside in the prefrontal cortex (PFC). As gait automaticity diminishes in older adults6, activation of the PFC during walking tasks increases. Lack of gait automaticity can interfere with community mobility, as the PFC is no longer free to process other information for navigating community environments. Another potential contributor to reduced community mobility is diminished locomotor adaptation. Specifically, older adults are slower at adjusting their movements while interacting with a new environment and have more difficulty switching motor patterns when transitioning across distinct walking conditions. This difficulty in switching motor patterns is related to cognitive switching ability, which is reliant upon similar subcortical-frontal processes that underlie motor control. While locomotor adaptation is reduced in normal aging, data from our lab indicates that older adults maintain plasticity and can improve locomotor adaptation. Our central hypothesis is that the ability to improve locomotor adaptation is greater in those with higher gait automaticity and greater integrity of the prefrontal-subcortical connections. The extent of gait automaticity can be tested by increasing the cognitive load during walking (e.g., completing a cognitive task while walking) and measuring the related PFC response. Small changes in PFC activity and motor performance in response to the imposed cognitive load indicate intact gait automaticity. Conversely, a large change in PFC activity to maintain motor performance with addition of a cognitive load indicates diminished gait automaticity. Locomotor adaptability can be measured by manipulating walking context on a split-belt treadmill where the legs are moving at different speeds. Adaptation rate to the split-belt environment can be measured as well as the ability to switch motor patterns from the split-belt to overground walking. Promising data from our labs (n=8) indicate that older participants improve locomotor adaptation after experiencing multiple transitions between the split condition (belts' speed ratio 2:1) and regular walking (belts' speed ratio 1:1). However, neither the underlying mechanisms nor the clinical relevance of such improvements are known. The investigators will test the following: 1) the extent of locomotor adaptation improvement in individuals aged 65 years and older; 2) the association between initial walking automaticity (i.e. less PFC activity while walking with a cognitive load) and prefrontal-subcortical function (measured via neuropsychological testing); and 3) whether improvements in locomotor adaptability result in improvements in the Functional Gait Assessment (FGA), a clinically relevant indicator of dynamic balance and mobility in older adults. To answer these questions, the investigators will combine innovative techniques from multiple laboratories at the University of Pittsburgh. Automatic motor control (Dr. Rosso's expertise) will be assessed by wireless functional near-infrared spectroscopy (fNIRS) of the PFC during challenged walking conditions (walking on an uneven surface and walking while reciting every other letter of the alphabet). fNIRS allows for real-time assessment of cortical activity while a participant is upright and moving by way of light-based measurements of changes in oxygenated and deoxygenated hemoglobin. Locomotor adaptation (Dr. Torres-Oviedo's expertise) will be evaluated with a split-belt walking protocol (i.e., legs moving at different speeds) that the investigators and others have used to robustly quantify motor adaptation capacity in older individuals and have shown to be reliant on cerebellar and basal ganglia function. The investigators will focus on two important aspects of locomotor adaptation that the investigators have quantified before: (Aim 1) rate at which individuals adapt to the new (split) walking environment and (Aim 2) capacity to transition between distinct walking patterns (i.e., the split-belt and the overground walking patterns), defined as motor switching. Adaptation rate and motor switching are quantified using step length asymmetry, which is the difference between a step length taken with one leg vs. the other. The investigators will focus on this gait parameter because it robustly characterizes gait adaptation evoked by split-belt walking protocols. Finally, the investigators will quantify participant's cognitive function (Dr. Weinstein's expertise) through neuropsychological battery sensitive to prefrontal-subcortical function. The investigators will mainly focus on evaluating 1) learning capacity reliant on cerebellar structures and 2) assessing executive function heavily reliant on PFC and, to a lesser extent, the basal ganglia. With this data, the investigators will be able to address the following Aims: Aim 1. Determine the association between improved locomotor adaptation rate and 1) individuals' gait automaticity and 2) cognitive function. Hypothesis: changes in adaptation rate will be predicted by initial walking automaticity and cerebellar-mediated learning capacity. This is predicated on the evidence that motor adjustments during split-belt walking depend on basal ganglia and cerebellar function. Aim 2. Determine the association between improved locomotor switching and individuals' gait automaticity and cognitive function. Hypothesis: initial walking automaticity and executive control will predict improvements in locomotor switching. This is predicated on the evidence that motor switching is directly associated with basal ganglia-dependent cognitive tasks such as set-shifting. Aim 3. Determine the extent to which improved locomotor adaptability could improve mobility. Hypothesis: changes in locomotor adaptability will not be exclusive to the laboratory context but will generalize to other locomotor tasks that require adaptability, as measured in the Functional Gait Assessment. These results will provide strong preliminary data for a future study to explore these associations in a larger sample with more comprehensive measures of mobility contributors, neuroimaging for integrity of key brain regions, and objective measures of community mobility. These results will identify novel contributors to loss of community mobility in older adults and could identify novel therapeutic targets for interventions that improve gait adaptation to prevent falls and enhance independence.