Prefrontal over-activation during walking in people with mobility deficits: Interpretation and functional implications
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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2022, Human Movement ScienceCitation 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).