Cortical activity during walking and balance tasks in older adults and in people with Parkinson’s disease: a structured review

An emerging body of literature has examined cortical activity during walking and balance tasks in older adults and in people with Parkinson’s disease, specifically using functional near infrared spectroscopy (fNIRS) or electroencephalography (EEG). This review provides an overview of this developing area, and examines the disease-specific mechanisms underlying walking or balance deficits. Medline, PubMed, PsychInfo and Scopus databases were searched. Articles that described cortical activity during walking and balance tasks in older adults and in those with PD were screened by the reviewers. Thirty-seven full-text articles were included for review, following an initial yield of 566 studies. This review summarizes study findings, where increased cortical activity appears to be required for older adults and further for participants with PD to perform walking and balance tasks, but specific activation patterns vary with the demands of the particular task. Studies attributed cortical activation to compensatory mechanisms for underlying age- or PD-related deficits in automatic movement control. However, a lack of standardization within the reviewed studies was evident from the wide range of study protocols, instruments, regions of interest, outcomes and interpretation of outcomes that were reported. Unstandardized data collection, processing and reporting limited the clinical relevance and interpretation of study findings. Future work to standardize approaches to the measurement of cortical activity during walking and balance tasks in older adults and people with PD with fNIRS and EEG systems is needed, which will allow direct comparison of results and ensure robust data collection/reporting. Based on the reviewed articles we provide clinical and future research recommendations

Neural Underpinnings of Walking Under Cognitive and Sensory Load: A Mobile Brain/Body Imaging Approach

Dual-task walking studies, in which individuals engage in an attentionally-demanding task while walking, have provided indirect evidence via behavioral and biomechanical measures, of the recruitment of higher-level cortical resources during gait. Additionally, recent EEG and imaging (PET, fNIRS) studies have revealed direct neurophysiological evidence of cortical contributions to steady-state walking. However, there remains a lack of knowledge regarding the underlying neural mechanisms involved in the allocation of cortical resources while walking under increased load. This dissertation presents three experiments designed to provide a greater understanding of the cortical dynamics implicated in processing load (top-down or bottom-up) during locomotion. Furthermore, we seek to investigate age-related differences in these neural pathways. These studies were conducted using an innovative EEG-based Mobile Brain/Body Imaging (MoBI) approach, combining high-density EEG, foot force sensors and 3D body motion capture as participants walked on a treadmill. The first study employed a Go/No-Go response inhibition task to evaluate the long-term test-retest reliability of two cognitively-evoked event-related potentials (ERPs), the earlier N2 and the later P3. Acceptable levels of reliability were found, according to the intraclass correlation coefficient (ICC), and these were similar across sitting and walking conditions. Results indicate that electrocortical signals obtained during walking are stable indices of neurophysiological function. The aim of the second study was to characterize age-related changes in gait and in the allocation of cognitive control under single vs. dual-task load. For young adults, we observed significant modulations as a result of increased task load for both gait (longer stride time) and for ERPs (decreased N2 amplitude and P3 latency). In contrast, older adults exhibited costs in the cognitive domain (reduced accuracy performance), engaged in a more stereotyped pattern of walking, and showed a general lack of ERP modulation while walking under increased load, all of which may indicate reduced flexibility in resource allocation across tasks. Finally, the third study assessed the effects of sensory (optic flow and visual perturbations) and cognitive load (Go/No-Go task) manipulations on gait and cortical neuro-oscillatory activity in young adults. While walking under increased load, participants adopted a more conservative pattern of gait by taking shorter and wider strides, with cognitive load in particular associated with reduced motor variability. Using an Independent Component Analysis (ICA) and dipole-fitting approach, neuro-oscillatory activity was then calculated from eight source-localized clusters of Independent Components (ICs). Significant modulations in average spectral power in the theta (3-7Hz), alpha (8-12Hz), beta (13-30Hz), and gamma (31-45Hz) frequency bands were observed over occipital, parietal and frontal clusters of ICs, as a function of optic flow and task load. Overall, our findings demonstrate the reliability and feasibility of the MoBI approach to assess electrocortical activity in dual-task walking situations, and may be especially relevant to older adults who are less able to flexibly adjust to ongoing cognitive and sensory demands while walking

Human spatial navigation in the digital era: Effects of landmark depiction on mobile maps on navigators’ spatial learning and brain activity during assisted navigation

Navigation was an essential survival skill for our ancestors and is still a fundamental activity in our everyday lives. To stay oriented and assist navigation, our ancestors had a long history of developing and employing physical maps that communicated an enormous amount of spatial and visual information about their surroundings. Today, in the digital era, we are increasingly turning to mobile navigation devices to ease daily navigation tasks, surrendering our spatial and navigational skills to the hand-held device. On the flip side, the conveniences of such devices lead us to pay less attention to our surroundings, make fewer spatial decisions, and remember less about the surroundings we have traversed. As navigational skills and spatial memory are related to adult neurogenesis, healthy aging, education, and survival, scientists and researchers from multidisciplinary fields have made calls to develop a new account of mobile navigation assistance to preserve human navigational abilities and spatial memory. Landmarks have been advocated for special attention in developing cognitively supportive navigation systems, as landmarks are widely accepted as key features to support spatial navigation and spatial learning of an environment. Turn-by-turn direction instructions without reference to surrounding landmarks, such as those provided by most existing navigation systems, can be one of the reasons for navigators’ spatial memory deterioration during assisted navigation. Despite the benefit of landmarks in navigation and spatial learning, long-standing literature on cognitive psychology has pointed out that individuals have only a limited cognitive capacity to process presented information for a task. When the learning items exceed learners’ capacity, the performance may reach a plateau or even drop. This leads to an unexamined yet important research question on how to visualize landmarks on a mobile map to optimize navigators’ cognitive resource exertion and thus optimize their spatial learning. To investigate this question, I leveraged neuropsychological and hypothesis-driven approaches and investigated whether and how different numbers of landmarks depicted on a mobile map affected navigators’ spatial learning, cognitive load, and visuospatial encoding. Specifically, I set out a navigation experiment in three virtual urban environments, in which participants were asked to follow a given route to a specific destination with the aid of a mobile map. Three different numbers of landmarks—3, 5, and 7—along the given route were selected based on cognitive capacity literature and presented to 48 participants during map-assisted navigation. Their brain activity was recorded both during the phase of map consultation and during that of active locomotion. After navigation in each virtual city, their spatial knowledge of the traversed routes was assessed. The statistical results revealed that spatial learning improved when a medium number of landmarks (i.e., five) was depicted on a mobile map compared to the lowest evaluated number (i.e., three) of landmarks, and there was no further improvement when the highest number (i.e., seven) of landmarks were provided on the mobile map. The neural correlates that were interpreted to reflect cognitive load during map consultation increased when participants were processing seven landmarks depicted on a mobile map compared to the other two landmark conditions; by contrast, the neural correlates that indicated visuospatial encoding increased with a higher number of presented landmarks. In line with the cognitive load changes during map consultation, cognitive load during active locomotion also increased when participants were in the seven-landmark condition, compared to the other two landmark conditions. This thesis provides an exemplary paradigm to investigate navigators’ behavior and cognitive processing during map-assisted navigation and to utilize neuropsychological approaches to solve cartographic design problems. The findings contribute to a better understanding of the effects of landmark depiction (3, 5, and 7 landmarks) on navigators’ spatial learning outcomes and their cognitive processing (cognitive load and visuospatial encoding) during map-assisted navigation. Of these insights, I conclude with two main takeaways for audiences including navigation researchers and navigation system designers. First, the thesis suggests a boundary effect of the proposed benefits of landmarks in spatial learning: providing landmarks on maps benefits users’ spatial learning only to a certain extent when the number of landmarks does not increase cognitive load. Medium number (i.e., 5) of landmarks seems to be the best option in the current experiment, as five landmarks facilitate spatial learning without taxing additional cognitive resources. The second takeaway is that the increased cognitive load during map use might also spill over into the locomotion phase through the environment; thus, the locomotion phase in the environment should also be carefully considered while designing a mobile map to support navigation and environmental learning

The Time-Budget Perspective of the Role of Time Dimension in Modular Network Dynamics during Functions of the Brain

Information processing plays a key role in the daily activities of human and nonhuman primates. Information processing in the brain, underlying behavior, is constrained by the four-dimensional nature of external physical surroundings. In contrast to three geometric dimensions, there are no known peripheral sensory organs for the perception of time dimension. However, the representation of time dimension in modular neural networks is critical for the brain functions that require interval timing or the temporal coupling of action with perception. Recent experimental and theoretical studies are shedding light on how the representation of time dimension in neural circuits plays a key role in the diverse functions of the brain, which also includes motor interactions with environment as well as social interactions, such as verbal and nonverbal communication. Although different lines of evidence strongly suggest that rhythmic neural activities represent time dimension in the brain, how the information represented by rhythmic activities is processed to time behavioral responses by the brain remains unclear. Theoretical considerations suggest that the rhythmic activities represent a physical aspect of the time dimension rather than the source of simple additive temporal units for coding time intervals in neural circuits

Plasticity of Brain Networks in a Randomized Intervention Trial of Exercise Training in Older Adults

Research has shown the human brain is organized into separable functional networks during rest and varied states of cognition, and that aging is associated with specific network dysfunctions. The present study used functional magnetic resonance imaging (fMRI) to examine low-frequency (0.008 < f < 0.08 Hz) coherence of cognitively relevant and sensory brain networks in older adults who participated in a 1-year intervention trial, comparing the effects of aerobic and non-aerobic fitness training on brain function and cognition. Results showed that aerobic training improved the aging brain's resting functional efficiency in higher-level cognitive networks. One year of walking increased functional connectivity between aspects of the frontal, posterior, and temporal cortices within the Default Mode Network and a Frontal Executive Network, two brain networks central to brain dysfunction in aging. Length of training was also an important factor. Effects in favor of the walking group were observed only after 12 months of training, compared to non-significant trends after 6 months. A non-aerobic stretching and toning group also showed increased functional connectivity in the DMN after 6 months and in a Frontal Parietal Network after 12 months, possibly reflecting experience-dependent plasticity. Finally, we found that changes in functional connectivity were behaviorally relevant. Increased functional connectivity was associated with greater improvement in executive function. Therefore the study provides the first evidence for exercise-induced functional plasticity in large-scale brain systems in the aging brain, using functional connectivity techniques, and offers new insight into the role of aerobic fitness in attenuating age-related brain dysfunction

Executive control of walking in people with Parkinson’s disease with freezing of gait

Background: Walking abnormalities in people with Parkinson’s disease (PD) are characterized by a shift in locomotor control from healthy automaticity to compensatory prefrontal executive control. Indirect measures of automaticity of walking (e.g., step-to-step variability and dual-task cost) suggest that freezing of gait (FoG) may be associated with reduced automaticity of walking. However, the influence of FoG status on actual prefrontal cortex (PFC) activity during walking remains unclear. Objective: To investigate the influence of FoG status on automaticity of walking in people with PD. Methods: Forty-seven people with PD were distributed into two groups based on FoG status, which was assessed by the New Freezing of Gait Questionnaire: PD-FoG (n=23; UPDRS-III=35) and PD+FoG (n=24; UPDRS-III=43.1). Participants walked over a 9m straight path (with a 180° turn at each end) for 80s. Two conditions were tested Off medication: single- and dual-task walking (i.e., with a concomitant cognitive task). A portable functional near-infrared spectroscopy system recorded PFC activity while walking (including turns). Wearable inertial sensors were used to calculate spatiotemporal gait parameters. Results: PD+FoG had greater PFC activation during both single and dual-task walking than PD-FoG (p=0.031). There were no differences in gait between PD-FoG and PD+FoG. Both groups decreased gait speed (p=0.029) and stride length (p<0.001) during dual-task walking compared to single-task walking. Conclusions: These findings suggest that PD+FoG have reduced automaticity of walking, even in absence of FoG episodes. PFC activity while walking seems to be more sensitive than gait measures in identifying reduction in automaticity of walking in PD+FoG

Neuroimaging of Human Balance Control: A Systematic Review

This review examined 83 articles using neuroimaging modalities to investigate the neural correlates underlying static and dynamic human balance control, with aims to support future mobile neuroimaging research in the balance control domain. Furthermore, this review analyzed the mobility of the neuroimaging hardware and research paradigms as well as the analytical methodology to identify and remove movement artifact in the acquired brain signal. We found that the majority of static balance control tasks utilized mechanical perturbations to invoke feet-in-place responses (27 out of 38 studies), while cognitive dual-task conditions were commonly used to challenge balance in dynamic balance control tasks (20 out of 32 studies). While frequency analysis and event related potential characteristics supported enhanced brain activation during static balance control, that in dynamic balance control studies was supported by spatial and frequency analysis. Twenty-three of the 50 studies utilizing EEG utilized independent component analysis to remove movement artifacts from the acquired brain signals. Lastly, only eight studies used truly mobile neuroimaging hardware systems. This review provides evidence to support an increase in brain activation in balance control tasks, regardless of mechanical, cognitive, or sensory challenges. Furthermore, the current body of literature demonstrates the use of advanced signal processing methodologies to analyze brain activity during movement. However, the static nature of neuroimaging hardware and conventional balance control paradigms prevent full mobility and limit our knowledge of neural mechanisms underlying balance control

More Automation and Less Cognitive Control of Imagined Walking Movements in High- Versus Low-Fit Older Adults

Using motor imagery, we investigated brain activation in simple and complex walking tasks (walking forward and backward on a treadmill) and analyzed if the motor status of older adults influenced these activation patterns. Fifty-one older adults (64–79 years of age) were trained in motor execution and imagery and then performed the imagination task and two control tasks (standing, counting backward) in a horizontal position within a 3T MRI scanner (first-person perspective, eyes closed). Walking backward as compared to walking forward required larger activations in the primary motor cortex, supplementary motor area, parietal cortex, thalamus, putamen, and caudatum, but less activation in the cerebellum and brainstem. Motor high-fit individuals showed more activations and larger BOLD signals in motor-related areas compared to low-fit participants but demonstrated lower activity in the dorsolateral prefrontal cortex. Moreover, parietal activation in high-fit participants remained stable throughout the movement period whereas low-fit participants revealed an early drop in activity in this area accompanied by increasing activity in frontal brain regions. Overall, walking forward seemed to be more automated (more activation in cerebellum and brainstem), whereas walking backward required more resources, e.g., for visual-spatial processing and sensorimotor control. Low-fit subjects in particular seemed to require more cognitive resources for planning and controlling. High-fit subjects, on the contrary, revealed more movement automation and a higher “attention span.” Our results support the hypothesis that high fitness corresponds with more automation and less cognitive control of complex motor tasks, which might help to free up cognitive resources

Cognitive-Motor Integration In Normal Aging And Preclinical Alzheimer's Disease: Neural Correlates And Early Detection

The objectives of the studies included in this dissertation were to characterize how the ability to integrate cognition into action is disrupted by both normal and pathological aging, to evaluate the effectiveness of kinematic measures in discriminating between individuals who are and are not at increased Alzheimer’s disease (AD) risk, and to examine the structural and functional neural correlates of cognitive-motor impairment in individuals at increased AD risk. The underlying hypothesis, based on previous research, is that measuring visuomotor integration under conditions that place demands on visual-spatial and cognitive-motor processing may provide an effective behavioural means for the early detection of brain alterations associated with AD risk. To this end, the first study involved testing participants both with and without AD risk factors on visuomotor tasks using a dual-touchscreen tablet. Comparisons between high AD risk participants and both young and old healthy control groups revealed significant performance disruptions in at-risk participants in the most cognitively demanding task. Furthermore, a stepwise discriminant analysis was able to distinguish between high and low AD risk participants with a classification accuracy of 86.4%. Based on the prediction that the impairments observed in high AD risk participants reflect disruption to the intricate reciprocal communication between hippocampal, parietal, and frontal brain regions required to successfully prepare and update complex reaching movements, the second and third studies were designed to examine the underlying structural and functional connectivity associated with cognitive-motor performance. Young adult and both low AD risk and high AD risk older adult participants underwent anatomical, diffusion-weighted, and resting-state functional connectivity scans. These data revealed significant age-related declines in white matter integrity that were more pronounced in the high AD risk group. Decreased functional connectivity in the default mode network (DMN) was also found in high AD risk participants. Furthermore, measures of white matter integrity and resting-state functional connectivity with DMN seed-regions were significantly correlated with task performance. These data support our hypothesis that disease-related disruptions in visuomotor control are associated with identifiable brain alterations, and thus behavioural assessments incorporating both cognition and action together may be useful in identifying individuals at increased AD risk

The role of the prefrontal cortex in the control of dual-task gait

Prefrontal cortex is frequently linked to dual-task gait performance; however, its precise role is unknown. The purpose of this thesis was to examine the role of prefrontal cortex in the control of dual-task gait. Using transcranial direct stimulation (tDCS) to alter prefrontal cortex activity, the influence of prefrontal cortex on dual-task gait performance and the corticospinal system was examined across four experiential studies using the guided activation framework of prefrontal cortex function (Miller and Cohen, 2001). The first study examined the role of cognitive task type and walking speed on stride time variability and trunk range of motion during dual-task walking. Results revealed the greatest dual-task cost on gait occurred when walking at a slow speed whilst simultaneously performing a serial subtraction task, compared to performance of a working memory task, providing a rationale for the use of this paradigm in later studies. The second study examined the effect of prefrontal tDCS on dual-task gait performance during both normal and slow walking. Anodal tDCS reduced the dualtask cost on both gait and cognitive task performance, and these effects were not dependent on walking speed. These results indicating that prefrontal tDCS may alter the allocation of cognitive control across tasks during dual-task gait, in accordance with established models of prefrontal cortex function. The third study examined the effect of prefrontal tDCS on corticospinal excitability and working memory performance. Results revealed that cathodal tDCS reduced corticospinal excitability. However, there was no effect of tDCS on working memory performance. Because prefrontal tDCS altered the activity in remote motor networks, these results indicated a possible mechanism by which prefrontal cortex exerts control over gait performance. In addition, because this study failed to replicate previous reports of working memory improvement following tDCS, these results also suggested a degree of inter-individual variability in response to tDCS. The final study examined the influence of walking modality and task difficulty on the effects of prefrontal tDCS on dual-task gait performance. tDCS altered the allocation of cognitive control during over-ground dual-task gait performance, and 3 these effects were mediated by task difficulty. In contrast to the second study, there was no effect of tDCS on treadmill dual-task gait. A secondary aim of the final study was to examine whether cognitive and walking task performance were coordinated. Results revealed that participants articulated answers during the initial swing phase of the gait cycle more frequently than other phases, indicating a degree of coordination between the performance of these tasks. Overall the finding of this thesis indicate that prefrontal cortex is involved in the allocation of cognitive control processes during dual-task walking, in accordance with the guided activation and flexible hub accounts of frontal cortex function (Miller and Cohen, 2001; Cole et al., 2013). These findings may have implications for the design and validation of strategies aimed at improving the cognitive control of gait