Elsevier

Human Movement Science

Volume 59, June 2018, Pages 46-55
Human Movement Science

Prefrontal over-activation during walking in people with mobility deficits: Interpretation and functional implications

https://doi.org/10.1016/j.humov.2018.03.010Get rights and content

Highlights

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    Prefrontal cortical activity during walking was assessed with fNIRS.

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    Elderly and stroke participants exhibit prefrontal over-activation during walking.

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    Prefrontal over-activation is associated with walking performance deficits.

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    The CRUNCH framework of cognitive performance may also fit the task of walking.

Abstract

Background

Control of walking by the central nervous system includes contributions from executive control mechanisms, such as attention and motor planning resources. Executive control of walking can be estimated objectively by recording prefrontal cortical activity using functional near infrared spectroscopy (fNIRS).

Objective

The primary objective of this study was to investigate group differences in prefrontal/executive control of walking among young adults, older adults, and adults post-stroke. Also assessed was the extent to which walking-related prefrontal activity fits existing cognitive frameworks of prefrontal over-activation.

Methods

Participants included 24 adults post-stroke with moderate to severe walking deficits, 15 older adults with mild gait deficits, and 9 young healthy adults. Executive control of walking was quantified as oxygenated hemoglobin concentration in the prefrontal cortex measured by fNIRS. Three walking tasks were assessed: typical walking, walking over obstacles, and walking while performing a verbal fluency task. Walking performance was assessed by walking speed.

Results

There was a significant effect of group for prefrontal activity (p < 0.001) during typical and obstacles walking tasks, with young adults exhibiting the lowest level of prefrontal activity, followed by older adults, and then adults post-stroke. In young adults the prefrontal activity during typical walking was much lower than for the verbal fluency dual-task, suggesting substantial remaining prefrontal resources during typical walking. However, in older and post-stroke adults these remaining resources were significantly less (p < 0.01). Cumulatively, these results are consistent with prefrontal over-activation in the older and stroke groups, which was accompanied by a steeper drop in walking speed as task complexity increased to include obstacles (p < 0.05).

Conclusions

There is a heightened use of prefrontal/executive control resources in older adults and post-stroke adults during walking. The level of prefrontal resource utilization, particularly during complex walking tasks like obstacle crossing, may approach the ceiling of available resources for people who have walking deficits. Prior cognitive research has revealed that prefrontal over-activation combined with limited prefrontal resources can lead to poor cognitive performance. The present study suggests a similar situation influences walking performance. Future research should further investigate the extent to which prefrontal over-activation during walking is linked to adverse mobility outcomes.

Introduction

Control of walking by the central nervous system can be broadly viewed as a balance between automaticity and executive locomotor control (Clark, 2015, Yogev-Seligmann et al., 2008). Automaticity refers to coordinated control of walking by lower levels of the neuraxis, including the spinal cord, brainstem, and cerebellum (Clark, 2015, Nielsen, 2003). Executive locomotor control refers to the use of attentional resources and motor planning to control walking, which serves to supplement automaticity under complex walking conditions such as obstacle crossing (Clark et al., 2014, Maidan et al., 2016). Executive resources may also be recruited as a compensatory mechanism in an attempt to preserve performance when other systems contributing to locomotion are impaired (Caliandro et al., 2012, Clark, 2015).

Functional near infrared spectroscopy (fNIRS) has emerged in the literature as a powerful tool to investigate cortical executive contributions to the control of walking (Holtzer et al., 2014, Perrey, 2014). Heightened metabolic activity in the prefrontal cortex measured by fNIRS has been shown to be closely linked to the increased demand for planning and attention during motor and cognitive tasks (Clark et al., 2014, Herrmann et al., 2006, Holtzer et al., 2011, Maidan et al., 2016, Ohsugi et al., 2013, Okamoto et al., 2004). However, when studying how the brain controls task performance, a notable complication is that either higher or lower levels of brain activity might convey a benefit depending on the context of the task and person. It is therefore necessary to work within a strong evidence-based framework. One such framework that has emerged from the cognitive aging literature is the Compensation-Related Utilization of Neural Circuits Hypothesis, or CRUNCH (Reuter-Lorenz & Cappell, 2008). The most prominent feature of CRUNCH with regard to brain activity in older (or neurologically impaired) individuals is brain over-activity at submaximal levels of task difficulty, which brings these individuals closer to the “ceiling” of brain activation resources. This brain over-activation is viewed as compensatory and beneficial to preserving task performance at lower task difficulty levels (Cabeza et al., 2002, Reuter-Lorenz and Cappell, 2008). However, as the brain activity ceiling is approached, performance suffers due to a lack of available remaining resources.

The present study used fNIRS to assess prefrontal/executive control of typical walking and walking over obstacles in young adults, elderly adults, and adults post-stroke. The primary objective was to investigate possible group differences in prefrontal over-activation, and to assess the extent to which walking-related prefrontal activity fits the CRUNCH framework. The first hypothesis was that prefrontal activity would significantly differ among groups (stroke > elderly > young) for the typical and obstacles walking tasks, consistent with prefrontal over-activation in people with walking deficits. The second hypothesis was that the groups with walking deficits would have fewer remaining prefrontal resources during typical and obstacles walking (stroke < elderly < young), as calculated relative to a demanding dual-task walking condition. This would add additional evidence of prefrontal over-activation during walking. These primary hypotheses were also supplemented with additional analyses to assess behavioral implications of prefrontal over-activation and to explore the time course of prefrontal activity during walking task performance (earlier versus later time periods). This study seeks to provide important new evidence and interpretation of prefrontal brain activity during walking, in order to assist with future development of mechanistic and intervention studies to enhance walking function in impaired populations.

Section snippets

Participants

Participants included a convenience sample of twenty-four adults post-stroke with moderate to severe gait deficits, fifteen elderly adults with mild gait deficits, and nine young healthy adults (Table 1). Inclusion criteria for adults post-stroke were the occurrence of a single unilateral stroke in the previous four years, with accompanying hemiparesis (lower extremity Fugl-Meyer Motor Assessment (FMA) score < 30) and moderate to severe gait deficits including 10 m walking speed <0.8 m/s.

Participant characteristics and effect on prefrontal activity

Group differences in participant characteristics are presented in Table 1. Prefrontal ΔO2Hb did not show any significant effect of hemisphere, nor hemisphere × task interaction for any group (p > 0.40). Prefrontal ΔO2Hb was also not significantly different when comparing subgroups of people with left and right hemisphere strokes (side of stroke, and side × task interaction; p > 0.22). Based on these results, ΔO2Hb was averaged across hemispheres for each person for subsequent analyses. The

Discussion

The primary finding from this study is that older adults and people post-stroke exhibit over-activation of prefrontal cortex during typical and obstacles walking tasks. For Hypothesis 1, prefrontal activity quantified as ΔO2Hb was highest in the post-stroke group, followed by elderly adults, and lowest in young healthy adults. Also noteworthy is that the elderly and stroke groups generally exhibited the expected reduction in ΔHHb (coinciding with increasing ΔO2Hb) that is a signature of

Conclusions

There is a heightened use of executive control resources in elderly and post-stroke adults during walking, as measured by prefrontal cortical oxygenation. The level of prefrontal resource utilization, particularly during complex walking tasks like obstacle crossing, might approach the ceiling of available resources for compromised populations and thereby exacerbate walking deficits. The present findings fit within the CRUNCH framework, but further research is warranted to more definitively

Funding

This research was supported by the US Department of Veterans Affairs Rehabilitation Research & Development Service (B1149R, B9252C, 0115BRRC-02), the National Institute on Aging via the University of Florida Claude Pepper Older Americans Independence Center (2P30-AG028740-06), National Institutes of Health/National Institute of Child Health and Human Development K12 (HD055929) Rehabilitation Research Career Development Program, and the Foundation for Physical Therapy via a Florence P. Kendall

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      Citation Excerpt :

      However, a novel brain imaging technique, functional near-infrared spectroscopy (fNIRS), facilitates direct measurement of brain activity during dynamic activities, such as balance (Hinderaker, Sylcott, Williams, & Lin, 2019; Lin, Barker, Sparto, Furman, & Huppert, 2017) and various walking tasks (Beurskens, Helmich, Rein, & Bock, 2014; Fraser, Dupuy, Pouliot, Lesage, & Bherer, 2016; Hawkins et al., 2018; Holtzer et al., 2011; Mirelman et al., 2017; Pelicioni, Tijsma, Lord, & Menant, 2019; Stuart, Alcock, Rochester, Vitorio, & Pantall, 2019; Stuart et al., 2018). Studies using fNIRS to study aging effects have investigated the prefrontal cortex (PFC) activation during various dual-task walking conditions (Beurskens et al., 2014; Fraser et al., 2016; Hawkins et al., 2018; Holtzer et al., 2011; Mirelman et al., 2017; Stuart et al., 2019). Three studies concluded older adults had increased PFC activation compared with younger adults during dual-task walking conditions (Hawkins et al., 2018; Mirelman et al., 2017; Stuart et al., 2019).

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