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Article

The Use of Augmented Reality on a Self-Paced Treadmill to Quantify Attention and Footfall Placement Variability in Middle-Aged to Older-Aged Adults with Multiple Sclerosis

by
Manuel E. Hernandez
1,2,3,4,*,
Roee Holtzer
5,6,
Meltem Izzetoglu
7 and
Robert W. Motl
8
1
Department of Biomedical and Translational Sciences, Carle Illinois College of Medicine, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA
2
Department of Health and Kinesiology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA
3
Neuroscience Program, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA
4
Beckman Institute, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA
5
Ferkauf Graduate School of Psychology, Yeshiva University, Bronx, NY 10461, USA
6
Department of Neurology, Albert Einstein College of Medicine, Bronx, NY 10461, USA
7
Electrical and Computer Engineering, Villanova University, Villanova, PA 19085, USA
8
Department of Kinesiology and Nutrition, College of Applied Health Sciences, University of Illinois Chicago, Chicago, IL 60612, USA
*
Author to whom correspondence should be addressed.
Sclerosis 2025, 3(1), 3; https://doi.org/10.3390/sclerosis3010003
Submission received: 16 October 2024 / Revised: 26 December 2024 / Accepted: 15 January 2025 / Published: 17 January 2025
(This article belongs to the Special Issue Neuropsychiatric and Quality of Life (QoL) Aspects of Multiple Sclerosis, 2nd Edition)
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Abstract

:
Background/Objectives: Footfall placement variability is associated with falls in older adults and neurological diseases. Thus, the study of dual-task gait impairment in middle-aged to older-aged adults with multiple sclerosis (MS) is clinically relevant, particularly in environments that mimic the obstacles experienced in daily ambulation. Methods: A total of 10 middle-aged to older-aged adults with MS (eight female, mean ± SD age = 56 ± 5 years), 12 healthy older adults (HOAs, nine female, age = 63 ± 4 years), and 10 healthy young adults (HYAs, five female, age = 22 ± 3) were asked to perform cued walking (CW) or obstacle walking (OW) tasks without or with a concurrent backward alphabet recitation task (CWT, OWT), or dual tasks. Gait performance and attentional demands were measured using hit rate, stride velocity, footfall placement bias and variance, and prefrontal cortex (PFC) oxygenated hemoglobin HbO levels. Results: A significant dual-task condition-by-cohort interaction was seen in footfall placement bias and variance as indicated by a higher footfall placement bias and variance in dual-task vs. single-task conditions seen in HOAs, in comparison to HYAs and adults with MS. Further, a significant walking condition-by-cohort interaction was seen in the HbO levels as indicated by the higher PFC HbO levels seen in OW vs. CW in adults with MS, compared to adults without MS. Conclusions: The decreased accuracy and increased attention in footfall placement to visual cues on the ground observed in adults with MS and HOAs, relative to HYAs, may provide a marker for gait impairment and fall risk in older adults with MS.

1. Introduction

Multiple sclerosis (MS) is an immune-mediated disease affecting the myelin, oligodendrocytes, axons, and neurons in the central nervous system [1]. Mobility and cognitive impairments are prevalent in adults with MS and in older adults [2,3,4,5]. Given the significant shift in the prevalence of MS among older age groups [6], the declines in mobility and cognition associated with both aging and MS pathology would be expected. Thus, the examination of the impact of co-occurring changes with aging and MS on cognitive and mobility function is imperative.
Footfall placement variability has been found to increase in persons with MS relative to the age-matched individuals [7]. Furthermore, gait variability has been found to increase with age [8], and with decreased cognitive and physical ability [9,10], or disability in adults with MS [11]. Given the clinical relevance of assessing gait variability in older adults due to its association with falls [12], the examination of footfall placement changes in middle-aged and older adults with MS is of importance.
Typical tests of gait function in persons with MS include the 25-foot walk, yet increased sensitivity may be achieved through the use of more challenging walking tasks [13]. This study examined cued walking (CW) and obstacle walking (OW) tasks in middle-aged and older adults with MS, as a means to increasing maneuverability demands by providing specific targets on the walking surface and unexpected obstacles instead of targets. Both CW and OW tasks would be expected to increase the cognitive demand of walking [14,15,16,17,18,19,20], as measured by prefrontal cortex (PFC) activity, as both tasks require visual attention to cues in the environment to help guide footfall placement, similar to navigating in an unfamiliar terrain.
The use of augmented reality (AR) or virtual reality (VR) on the cognitive and motor rehabilitation of persons with MS has demonstrated positive outcomes [21,22,23,24]. As VR and AR allow for tasks to be tailored to the individual’s functional capacity, the combination of these technologies with walking tasks provide an opportunity to personalize rehabilitation for a wide array of populations, including adults with MS [23]. However, a further evaluation on older adults with MS may be beneficial to identify modifiable changes to target in future interventions.
Dual tasking refers to the concurrent performance of two attention-demanding tasks. Studies have typically suggested that the performance of at least one of the tasks may be poorer when dual tasking, but this is dependent on the difficulty of the tasks for older adults and adults with MS [25,26]. Visually guided walking with irregular cues has demonstrated increased demands, relative to regular cues or normal walking [14], and particularly while introducing obstacles [27,28,29]. Prior work has demonstrated that dual-task walking increases PFC activation in adults with MS and older adults [30,31,32,33,34]. In particular, verbal recitation tasks have been commonly used in divided attention paradigms in older adults with and without neurological conditions [31]. Furthermore, the performance of backward alphabet recitation tasks has demonstrated increased PFC activation while walking in adults with and without MS [13]. However, the impact of divided attention walking during obstacle navigation has not been explored in older adults with MS. Thus, by comparing and contrasting the impact of divided attention walking while guiding footfalls to irregular targets or navigating obstacles in older persons with MS, we may better understand some of the challenges they encounter in community ambulation [35,36].
Differential changes in the association between fronto-striatal integrity and lesion load in older adults with and without MS highlight the impact that lesion load has on mobility function in older adults with MS [37]. In particular, a higher whole brain lesion volume was associated with higher odds of mobility impairment, as evaluated by a score above 10 in the short physical performance battery, in older adults with MS but not in healthy older adults [37]. Evidence suggests that functional reorganization may explain the limited relationship between tissue degradation and the physical and cognitive deficits in adults with MS [38]. However, increased cortical recruitment may not always be beneficial for persons with MS [39,40]. Compensatory cortical activation is characterized by increased cortical activation in the PFC during cognitive tasks, which may compensate for tissue damage, and thus reduce the expected clinical effects of MS [38]. The compensatory cortical activation theory would suggest increased PFC activation in adults with MS and in older adults, relative to younger adults, during dual-task walking conditions, while similar performances would be observed. Alternatively, the increase in PFC activation in persons with MS and in older adults, relative to younger adults, while gait performance is decreased, would be consistent with a decrease in neural efficiency [41]. However, both compensatory cortical activation and decreases in neural efficiency can be present within the same person, depending on the difficulty of the task.
The objective of this study was to examine the impact of age and MS on the footfall placement variability and PFC activation to AR targets while dual tasking using functional near-infrared spectroscopy (fNIRS). fNIRS provides a reliable mobile neuroimaging technique for evaluating cortical activation while walking [31]. In the current study, we hypothesized that aging and MS would lead to increases in PFC activity, particularly in dual-task walking conditions and when navigating obstacles. Furthermore, we hypothesized that aging and MS would lead to a decreased performance, as evaluated by decreases in hit rate and stride velocity and increases in footfall placement bias and variance in dual-task walking conditions and when navigating obstacles. This study allowed us to evaluate if neural efficiency or neural compensation provided a better framework for explaining the differences in complex walking tasks.

2. Materials and Methods

2.1. Participants

The participants were recruited from the local community and from previous MS studies at the University of Illinois Urbana-Champaign. The participants consisted of 10 middle-aged to older-aged adults with MS (MS, 8 females), 12 healthy older adults (HOAs, 9 females), and 10 healthy young adults (HYAs, 5 females). A structured telephone interview was administered to potential participants to obtain their verbal consent, assess their medical history, and rule out dementia using the cut-off of 18 or above from the 13-item Telephone Interview for Cognitive Status (TICS-M) [42], based on prior findings indicating that 50 percent of older adults with a range of 19–28 had a diagnosis of amnesic mild cognitive impairment [43]. All participants with MS were relapse-free for the past 30 days and had mild to moderate disability, as evaluated by the Kurtzke Expanded Disability Status Scale (EDSS, range = 1–6, Median = 3.75, IQR = 0.875) [44]. The EDSS was evaluated through a neurological examination that was administered by a Neurostatus-certified examiner. HYAs and HOAs were included in the study if they had no physical disabilities, neurological diseases, or cardiovascular conditions. All participants were 18 years of age or older, had no lower limb injury within the last 6 months, were medically stable, and had normal or corrected to normal vision. The exclusion criteria for this study included left-handedness, as evaluated by the Edinburgh handedness questionnaire [45], lower limb injury or any neurological disease in addition to MS for the individuals with MS. The characteristics of the individuals are given in Table 1. This study was approved by the Institutional Review Board of the University of Illinois at Urbana-Champaign, and the participants provided written informed consent.

2.2. Procedure

The participants performed cued walking (CW), obstacle walking (OW), CW while talking (CWT), and OW while talking (OWT) trials on a 3 m self-paced instrumented treadmill (C-Mill; Motekforce Link, Culemborg, The Netherlands) while wearing a ceiling-mounted harness for safety (See Figure 1). During each trial, the participants wore an fNIRS sensor headband to monitor the changes in their hemodynamic activity in the PFC. For the CW trials, the participants were asked to step as accurately as possible to the center of each augmented reality target, which was rectangular in size and based on participants’ self-reported shoe size, on the surface of the treadmill belt, while keeping a comfortable pace. For the OW trials, infrequent obstacles were unexpectedly provided at a rate of under 30% of all targets and were presented as diagonal hashmarks on the same rectangular target, along with the targets. In OW trials, participants were asked to step as accurately as possible to the center of each augmented reality target while avoiding obstacles (see Figure 1). For both the CWT and the OWT trials, participants were asked to recite alternate letters of the alphabet backwards (e.g., Z, X, V, T, etc.) while performing the CW or OW task at the same time. The participants were instructed to pay equal attention to the cognitive task (reciting alternating letters of the alphabet backward) and the motor task (cued walking or obstacle walking). For all tasks, visual feedback was provided (i.e., a target or obstacle was provided) to help guide foot positioning, which was based on an individual’s average step length and step width during the time leading up to each task. For all tasks, participants had to look down to see the targets and obstacles while walking on the treadmill. Targets or obstacles were placed one step away from the leading foot when they first appeared on the belt and positioned based on an individual’s capacity, as noted above. Each trial consisted of 30 s to build up to the self-selected, comfortable speed, with the order pseudorandomized, with dual-task or single-task tests being randomized, and cued walking tasks occurring before obstacle walking tasks, to control for difficulty. The testing lasted for 30 s and was followed by a 15 s period to safely decelerate. After each trial, there was a brief rest period before resuming each baseline. Each CWT and OWT trial consisted of a different and randomized letter to start the backward alphabet recitation. There was also a 10 s baseline before each trial, where the participants were asked to stand still and count silently, starting from 1, until instructed to stop. Prior to testing, the participants were provided a practice session with both the cognitive task and self-paced walking on the treadmill for minimizing learning effects.

2.3. Baseline Cognitive and Mobility Function Assessments

The Repeatable Battery for the Assessment of Neuropsychological Status (RBANS) was used to assess overall cognitive function. The RBANS is a brief cognitive test with several alternate forms that measures attention, language, visuospatial skills, and immediate and delayed memory. It also provides a total index score for global cognitive function and is useful for the detection and characterization of dementia in older adults [46].
The Short Physical Performance Battery (SPPB) was used to assess mobility function [47]. The SPPB consists of balance, walking, and repeated sit-to-stand tasks. The SPPB is a validated and reliable assessment tool for quantifying mobility function in older adults with MS [48].

2.4. Data Collection

An fNIRS Imager 1000 series (fNIRS Devices, LLC, Potomac, MD, USA) system was used to monitor the changes in the hemodynamic activity in the PFC of participants during all walking tasks. As described in prior work [49,50], the fNIRS system consisted of a light weight and flexible sensor consisting of four LED light sources and 10 photodetectors with a 2.5 cm source-detector separation distance, which provided a coverage of the forehead with 16 voxels at a 2 Hz sampling rate. The light sources (Epitex Inc., Kyoto, Japan; type L4X730/4X805/4X850-40Q96-I) on the sensor contained three built-in LEDs with peak wavelengths at 730, 805, and 850 nm. The photodetectors (Bur Brown, type OPT101) are monolithic photodiodes with a single supply transimpedance amplifier. The sensor was placed on the participants’ forehead, with the vertical axis of the sensor aligned between the eyes and the bottom of the sensor just above the eyebrows, such that the bottom row of voxels was aligned with the FP1 and FP2 marker locations from the international 10–20 system, as described previously. E-Prime (Psychology Software Tools, Inc., Sharpsburg, PA, USA) was used to synchronize the start and stop of each walking trial and baseline with the fNIRS system. The raw force plate and belt speed data were collected from the instrumented treadmill at a 500 Hz sampling rate using the CueFors 2 software (Motekforce Link, Culemborg, The Netherlands). Custom scripts in MATLAB (MathWorks, Natick, MA, USA) were used to calculate the stride velocity, target hit rate, footfall placement bias, as measured by the mediolateral (ML) difference between the target’s center and center of pressure position (ML Error), and variance, as measured by the standard deviation (SD) of the footfall placement bias (ML Error SD). The hit rate was calculated by measuring the percentage of targets that were successfully reached, as measured by the midstance COP position being within the boundary of the provided target. The outcome measures were focused on ML direction, given the prior evidence of increased ML postural sway in adults with MS, [51] altered trunk variability and increased trunk velocity in the ML direction while walking, [52] and increased gait variability while approaching obstacles while walking in adults with MS [53].

2.5. Data Analysis

The data were processed by an offsite researcher who was uninvolved in the data collection and other experimental procedures (i.e., blinded fNIRS data analysis). The data from each of the 16 fNIRS voxels, under each of the experimental conditions, were carefully inspected and removed from analysis if saturation or dark current conditions were identified. Wavelet denoising with a Daubechies 5 (db5) wavelet was applied to the raw intensity measurements at the 730 and 850 nm wavelengths for spiky noise suppression [54]. The changes in HbO were calculated from those artifact-removed raw intensity measurements using modified Beer–Lambert law (MBLL) as previously described [55]. In MBLL, we used the previously published wavelength and chromophore-dependent molar extinction coefficients (ε) by Prahl, and age and wavelength adjusted the differential pathlength factor (DPF) [54]. To remove possible baseline shifts and to suppress physiological artifacts such as respiration and Mayer waves, we first applied Spline filtering, followed by a finite impulse response low-pass filter with a cut-off frequency at 0.08 Hz [54]. In the current experiment, HbO values were used to characterize changes in the PFC during the CW, OW, CWT, and OWT conditions since they are more reliable and sensitive to locomotion-related changes in cerebral blood flow [56]. Also, using one index for task-related hemodynamic changes in the PFC reduced the number of comparisons and thus the probability of increased Type I errors. To determine the relative task-related changes in HbO values, the average in each walking condition was subtracted by the average baseline value during quiet standing prior to each condition. Individual mean HbO2 data were extracted separately for CW, OW, CWT and OWT.

2.6. Statistical Analysis

Descriptive statistics were provided to evaluate the differences in demographic characteristics and functional assessment performance. The differences in demographic characteristics or functional performance were evaluated using a one-way analysis of variance (ANOVA) or Chi-square test. Full-factorial linear mixed effects models were used with the cohort (HYAs, HOAs, or MS) as the three-level model between subject factors, walking condition (CW vs. OW) as a two-level model repeated within-subject factor, dual-task condition (single vs. dual task) as a two-level model repeated within-subject factor, and stride velocity, target hit rate, footfall placement bias and variance as the dependent measures. A random intercept was included in the model to allow the entry point to vary across individuals. As a secondary analysis, we examined the correlation between behavioral performance outcome measures in this AR protocol and disability and cognitive function using a Spearman correlation.
A full factorial linear mixed effects model with the cohort (HYAs, HOAs, or MS) as the three-level model between subject factor, walking condition (CW vs. OW) as a two-level model repeated within-subject factor, dual-task condition (single vs. dual task) as a two-level model repeated within-subject factor, and HbO levels in each of the 16 voxels as the dependent measure, while controlling for the repeated measures across the 16 voxels, was used to examine whether oxygenation levels increased as a function of the introduction of obstacles or dual-task interference. As random effects, random intercepts by individuals across voxels were included. Post hoc t-tests were run to identify the significant differences between groups, walking conditions, and dual-task conditions. For all statistical analyses in this study, the study-wise level of significance was set at p = 0.05. The data were visually inspected for model assumptions. Statistical analyses were performed using R 4.4.0 and lme4.

3. Results

The three cohorts differed in age and mobility function, as evaluated by the SPPB (see Table 1). HYAs, HOAs, and adults with MS had similar heights, weights, and cognitive functions (see Table 1). The mean (SD) RBANS total index score of 98 (13) to 106 (11) across groups was indicative of the average cognitive function.

3.1. Behavioral Performance

Overall, the results from linear mixed models showed a significant walking condition effect (F = 44.5, p < 0.001) and a walking condition-by-cohort effect (F = 3.7, p = 0.029) was observed on hit rate, such that the hit rate was decreased when going from cued walking to obstacle walking conditions, and particularly for HOAs, as seen in Figure 2. Overall, there was a dual-task condition main effect whereby stride velocity was decreased in dual-task compared with single-task walking conditions across both groups of participants (F = 17.6, p < 0.001). In addition, there was a significant dual-task-by-walking condition interaction effect (F = 4.9, p = 0.030), where stride velocity was decreased in dual-task conditions in cued walking but not obstacle walking conditions. Furthermore, persons with MS demonstrated a higher footfall placement bias, as measured by the ML error, than adults without MS, given the significant cohort effect (F = 4.2, p = 0.025). There was also a significant dual-task condition-by-cohort interaction observed (F = 4.8, p = 0.010), where HOAs demonstrated a higher ML error in dual-task vs. single-task conditions, in comparison to HYAs and adults with MS. In addition, adults with MS had higher footfall placement variance, as measured by the standard deviation of the footfall placement bias (ML Error SD), when compared to HYAs and HOAs (F = 3.7, p = 0.034). There was also a significant walking condition effect, such that obstacle walking resulted in higher ML Error SD when compared to cued walking conditions (F = 18.1, p < 0.001). Lastly, there was a significant dual-task condition-by-cohort interaction observed (F = 4.5, p = 0.014), such that HOAs demonstrated a higher ML Error SD in dual-task walking vs. single-task walking conditions, compared to HYAs and adults with MS. No other significant differences were observed.
Post hoc t-tests confirmed a significant lower hit rate in obstacle walking vs. cued walking conditions, with and without a dual task, in HYAs (p < 0.05) and HOAs (p < 0.001). A significant lower stride velocity was seen in CWT vs. CW tasks in all groups (p < 0.05 for adults with MS, and p < 0.01 for HYAs and HOAs) and in OW vs. CW tasks in HOAs (p < 0.05). A significant increase in ML error was seen in adults with MS vs. HOAs in both CW (p < 0.05) and OW (p < 0.01) tasks, and in OW vs. OWT task in adults with MS (p < 0.05). A significant increase in ML Error SD was seen in adults with MS vs. HYAs during both CWT and OWT tasks (p < 0.05), in OWT vs. OW tasks in HOAs (p < 0.05), and in OW vs. CW tasks in HYAs (p < 0.01) and adults with MS (p < 0.05).

3.2. Prefrontal Cortex Oxygenated Hemoglobin Levels

The PFC HbO levels in HYAs, HOAs, and adults with MS during CW, CWT, OW, and OWT conditions are depicted in Figure 3. The results from the linear mixed model suggested a main effect of the dual-task condition such that PFC HbO levels were higher in dual-task walking vs. single-task walking condition (F = 142.4, p < 0.001). Significant cohort effects were observed (F = 3.9, p = 0.020), such that adults with MS and HOAs demonstrated higher PFC HbO levels compared to HYAs. The results further indicated a significant walking condition-by-cohort interaction such that there were higher PFC HbO levels in obstacle vs. cued walking in adults with MS, compared to adults without MS. No further significant differences were observed.
Post hoc t-tests confirmed a significant increase in PFC HbO levels in every dual-task vs. single-task condition (p < 0.001). Further, a significant increase in PFC HbO levels in adults with MS vs. HYAs in OW and OWT (p < 0.05) and a significant increase in PFC HbO levels in HOAs vs. HYAs in OW (p < 0.01) was observed. Lastly, a significant increase in PFC HbO levels was seen in adults with MS between CWT and OWT, while a decrease was seen in HYAs (p < 0.05).

3.3. Association Between Behavioral Performance and Disability and Cognitive Function in MS

Overall, the behavioral performance in this AR protocol was found to be associated with both disability and cognitive function in adults with MS. Specifically, a negative association was observed between stride velocity and disability, as evaluated by the EDSS (−0.46, p = 0.003). Furthermore, there exist significant correlations between cognitive function, as evaluated by the RBANS, and both ML Error SD (−0.52, p < 0.001) and ML error (−0.55, p < 0.001). No other significant associations were observed.

4. Discussion

This study investigated the impact of age and MS on the footfall placement variability and PFC activation to AR targets while dual tasking. To our knowledge, this is the first study to examine PFC activation patterns in persons with MS during dual-task cued and obstacle walking conditions. We hypothesized that aging and MS would lead to increases in PFC and a decrease in neural efficiency [41], particularly in dual-task walking conditions and when navigating obstacles, which were partly supported by the higher PFC HbO levels seen in obstacle vs. cued walking in adults with MS, compared to adults without MS (Figure 3). We further hypothesized that aging and MS would lead to decreased performance, as evaluated by decreases in hit rate and stride velocity and increases in footfall placement bias and variance in dual-task walking conditions and when navigating obstacles, which was partly supported by the decreased hit rate when going from cued walking to obstacle walking conditions, and particularly for HOAs and higher footfall placement bias (ML Error) and variance (ML Error SD) in dual-task vs. single-task conditions seen in HOAs, in comparison to HYAs and adults with MS (Figure 2).

4.1. Addition of Obstacles Increases PFC Activity and Footfall Placement Variability

The overall findings of increased PFC activation during obstacle walking, relative to cued walking, are consistent with a larger amplitude in the fronto-central activity when reacting to unexpected obstacles [57,58,59], and increased PFC activation when obstacles are unexpected [60] and combined with a concurrent working memory task [61]. However, while both HOAs and adults with MS demonstrated an increase in PFC activation when going from cued to obstacle walking tasks, a similar level of PFC activation was seen in HYAs, in contrast to prior findings examining obstacles relative to normal walking in young adults [60], which may be due to our use of irregular AR cues that decreased gait automaticity in younger adults in the cued walking condition [62]. Furthermore, the addition of unexpected obstacles to cued walking resulted in a decreased hit rate of AR targets while the successful hits of the AR targets demonstrated increased footfall placement variance, which is consistent with motor-cognitive interference [63,64].

4.2. Differential Effect of Obstacles on PFC Activity in Older Adults and MS

Consistent with a decrease in neural efficiency [41], a significant walking condition-by-cohort interaction was seen in both PFC activation and hit rate. Specifically, a higher PFC activity was seen in OWT vs. CWT in adults with MS, but lower PFC activity in OWT vs. CWT in HYAs, while both HOAs and adults with MS had lower hit rates in obstacle vs. cued walking conditions. Interestingly, all of the groups maintained a similar stride velocity between cued and obstacle walking tasks. Thus, a similar amount of time was available to process visual cues and plan footfall placement, but the concurrent obstacles elicited increased PFC activity in older adults and adults with MS.

4.3. Increases in PFC Activity and Decreases in Performance While Dual-Task Walking

The addition of a backward alphabet recitation task to cued and obstacle walking consistently resulted in an increase in PFC activity and decrease in stride velocity (see Figure 2 and Figure 3). The backward alphabet recitation task presented a mental tracking task that required participants to hold on to information in working memory while performing a mental process that overlaps with the neural networks and cortical and sub-cortical regions involved in the control of gait. Prior work has demonstrated a wide range of activations due to backward recitations of the alphabet, including in the parietal, temporal, frontal, and occipital cortical regions, as well as the insula, cingulate gyrus, and thalamus [65]. In particular, the frontal and temporal areas overlap with areas used to control gait [66,67], while the intraparietal sulcus, implicated in the control of gait and movement based on visual information [68], is also active in backward recitation tasks [65].
While no differential increase in PFC activation was observed in adults with MS and HOAs, relative to HYAs, during dual-task walking conditions, increased PFC activation was observed during dual-task vs. single-task walking across all cohorts, which is consistent with prior work [30]. Further, stride velocity was decreased when adding a dual task to cued walking conditions, which is consistent with motor-cognitive interference [63,64]. Given the significant dual-task-by-cohort interactions in footfall placement bias and variance, the findings are consistent with limitations in adaptation, where PFC activity may be starting to be limited in further increases. However, further work is needed to identify the potential “crunch” point at which older adults with and without MS are unable to maintain a similar level of performance relative to younger adults. This tradeoff is known as the compensation-related utilization of neural circuits hypothesis, or CRUNCH [69], and has been observed in prior work examining walking and talking in adults with MS [13].

4.4. Implications of Current Findings

While walking in the community, such as when shopping for groceries in the local market, older adults with and without MS may often find themselves having to navigate tight quarters and unexpected obstacles while concurrently performing a cognitive task. Thus, the examination of concurrent motor and cognitive tasks to cued walking tasks, which mimic some of the challenges encountered in walking in our communities, provided an opportunity to further our understanding of the control of gait. The overactivation of the PFC during CW and OW tasks in HOAs and adults with MS, relative to HYAs (Figure 3), is consistent with a “supply and demand” framework [70], where the use of visual cues to guide footfall placement requires additional attentional resources in both older adults and adults with MS, due to structural and functional brain changes due to age and MS. The “supply and demand” framework posits that older adults increasingly rely on cognitive brain processes for motor control due to functional and structural changes in the central nervous system, while attentional capacity and other relevant cognitive resources are reduced.
The current AR protocol was partly sensitive to the differences in disability in adults with MS, as demonstrated by the association between stride velocity and disability. Further, ML footfall placement variability was found to be negatively associated with cognitive function in MS, which merits further exploration. Given the potential impact of cognitive fatigue in MS, further work should examine its potential impact on footfall placement variability in repeated trials.

4.5. Study Limitations

The examination of only the PFC is a limitation of this study, as the control of locomotion is dependent on numerous brain regions and networks outside of the PFC, such as the spinal cord, brainstem, cerebellum, basal ganglia, and motor cortex [63,64,65]. Furthermore, as we are limited by fNIRS to record from only cortical areas, or in a limited part of the PFC, the extent of task-related, age-related or MS-related changes in oxygenation levels observed in this study may be limited. Future work should examine gait variability changes in community ambulation, while controlling for environmental factors. Furthermore, future work should evaluate the feasibility of partial body weight support therapy or additional dual-task training on improving neural efficiency or behavioral performance, including gait variability, in older adults with MS. While dual-task paradigms such as the alternate-letter alphabet task, have been validated in persons with MS [12], more work is needed to further establish the reliability and validity of the existing walking paradigm in persons with MS. Given that the specific subtype of MS nor medications taken by participants were considered, future work should evaluate if MS-subtype or specific use of medications alter findings. Finally, the small sample and heterogeneity of participant characteristics are limitations that restrict the generalization and interpretation of these results to older adults with MS or other neurological conditions, such as Parkinson’s disease.

5. Conclusions

In summary, this study provided the first evidence that oxygenation levels are increased in the PFC of middle-aged to older adults with MS in OWT, when compared to healthy young and older adults. Furthermore, a decreased hit rate was seen when going from cued walking to obstacle walking conditions, particularly for HOAs, and higher footfall placement bias (ML Error) and variance (ML Error SD) in dual-task vs. single-task conditions were seen in HOAs, in comparison to HYAs and adults with MS. Consistent with prior findings of increased PFC activation during obstacle walking and decreases in neural efficiency, we found a significant walking condition-by-cohort interaction in both PFC activation and hit rate. These findings suggest that older adults with MS may be compensating for decreased efficiency by ramping up PFC activity in divided-attention obstacle walking tasks. Lastly, the decreased accuracy and increased attention in footfall placement to visual cues on the ground found in adults with MS and HOAs, relative to HYAs, may provide a marker for gait impairment and fall risk in older adults with MS.

Author Contributions

Conceptualization, M.E.H.; methodology, M.E.H., R.H., M.I. and R.W.M.; formal analysis, M.E.H. and M.I.; investigation, M.E.H. and R.W.M.; writing—original draft preparation, M.E.H., R.H., M.I. and R.W.M.; writing—review and editing, M.E.H., R.H., M.I. and R.W.M.; visualization, M.E.H.; supervision, M.E.H.; project administration, M.E.H.; All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki and approved by the Institutional Review Board (or Ethics Committee) of the University of Illinois Urbana-Champaign (protocol 15674, approved on 14 July 2022).

Informed Consent Statement

Informed consent was obtained from all of the subjects involved in the study.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

Acknowledgments

We would like to thank all of the participants that contributed to this study, as well as the members of the Mobility and Fall Prevention Research Lab that contributed to the data collection.

Conflicts of Interest

Izzetoglu has a minor share in the fNIRS device. All other authors declare no conflicts of interest to report in relation to the current article. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. Schematic of experimental setup with (A) layout of fNIRS sensor and its 16 voxel locations on prefrontal cortex; (B) equipment used during cued walking condition (cues are indicated using red rectangles); and (C) outline of experimental session, with baseline collection of Kurtzke Expanded Disability Status Scale (EDSS), Short Physical Performance Battery (SPPB), and the Repeatable Battery for the Assessment of Neuropsychological (RBANS); practice session of backward recitation cognitive task and self-paced treadmill walking; and pseudorandomized walking tasks that consisted of cued walking (CW), obstacle walking (OW), CW while talking (CWT), and OW while talking (OWT).
Figure 1. Schematic of experimental setup with (A) layout of fNIRS sensor and its 16 voxel locations on prefrontal cortex; (B) equipment used during cued walking condition (cues are indicated using red rectangles); and (C) outline of experimental session, with baseline collection of Kurtzke Expanded Disability Status Scale (EDSS), Short Physical Performance Battery (SPPB), and the Repeatable Battery for the Assessment of Neuropsychological (RBANS); practice session of backward recitation cognitive task and self-paced treadmill walking; and pseudorandomized walking tasks that consisted of cued walking (CW), obstacle walking (OW), CW while talking (CWT), and OW while talking (OWT).
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Figure 2. Mean (SEM) of hit rate (top left), stride velocity (top right), ML error (bottom left), and ML error SD (bottom right) across different walking tasks and cohorts. Note: CW = cued walking; CWT = cued walking while talking; OW = obstacle walking; OWT = obstacle walking and talking; HYAs = healthy young adults; HOAs = healthy older adults; and MS = middle-aged to older-aged adults with MS.
Figure 2. Mean (SEM) of hit rate (top left), stride velocity (top right), ML error (bottom left), and ML error SD (bottom right) across different walking tasks and cohorts. Note: CW = cued walking; CWT = cued walking while talking; OW = obstacle walking; OWT = obstacle walking and talking; HYAs = healthy young adults; HOAs = healthy older adults; and MS = middle-aged to older-aged adults with MS.
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Figure 3. Mean (SEM) pre-frontal cortex (PFC) oxygenated hemoglobin (HbO) levels of healthy young adults (HYAs), healthy older adults (HOAs), and middle-aged to older-aged adults with MS (MS) across cued walking (CW), cued walking while talking (CWT), obstacle walking (OW), and obstacle walking while talking (OWT) conditions.
Figure 3. Mean (SEM) pre-frontal cortex (PFC) oxygenated hemoglobin (HbO) levels of healthy young adults (HYAs), healthy older adults (HOAs), and middle-aged to older-aged adults with MS (MS) across cued walking (CW), cued walking while talking (CWT), obstacle walking (OW), and obstacle walking while talking (OWT) conditions.
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Table 1. Demographics and functional assessments.
Table 1. Demographics and functional assessments.
VariableHYA (n = 10)HOA (n = 12)MS (n = 10)p Value
MeanSDMeanSDMeanSD
Age (years)21.93.463.14.456.25.1<0.001
Height (m)1.70.11.70.091.70.090.942
Weight (kg)73.115.577.61870.49.60.536
RBANS98.619.1105.611.398.113.40.411
SPPB (0–12)11.50.511.60.710.21.80.012
NumberPercentNumberPercentNumberPercent
Females550.0975.0880.00.075
Note: HYAs = healthy younger adults; HOAs = healthy older adults; MS = multiple sclerosis; RBANS = Repeatable Battery for the Assessment of Neuropsychological Status; SPPB = Short Physical Performance Battery.
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Hernandez, M.E.; Holtzer, R.; Izzetoglu, M.; Motl, R.W. The Use of Augmented Reality on a Self-Paced Treadmill to Quantify Attention and Footfall Placement Variability in Middle-Aged to Older-Aged Adults with Multiple Sclerosis. Sclerosis 2025, 3, 3. https://doi.org/10.3390/sclerosis3010003

AMA Style

Hernandez ME, Holtzer R, Izzetoglu M, Motl RW. The Use of Augmented Reality on a Self-Paced Treadmill to Quantify Attention and Footfall Placement Variability in Middle-Aged to Older-Aged Adults with Multiple Sclerosis. Sclerosis. 2025; 3(1):3. https://doi.org/10.3390/sclerosis3010003

Chicago/Turabian Style

Hernandez, Manuel E., Roee Holtzer, Meltem Izzetoglu, and Robert W. Motl. 2025. "The Use of Augmented Reality on a Self-Paced Treadmill to Quantify Attention and Footfall Placement Variability in Middle-Aged to Older-Aged Adults with Multiple Sclerosis" Sclerosis 3, no. 1: 3. https://doi.org/10.3390/sclerosis3010003

APA Style

Hernandez, M. E., Holtzer, R., Izzetoglu, M., & Motl, R. W. (2025). The Use of Augmented Reality on a Self-Paced Treadmill to Quantify Attention and Footfall Placement Variability in Middle-Aged to Older-Aged Adults with Multiple Sclerosis. Sclerosis, 3(1), 3. https://doi.org/10.3390/sclerosis3010003

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