The current study applied fNIRS imaging to assess whether older adults demonstrated changes in prefrontal cerebral oxygenation and behaviour while walking with cognitive tasks of increasing difficulty. The aims of this study were two-fold. Firstly, to analyze neural and behavioural measures to better understand neural compensation mechanisms during dual-tasks of different difficulty levels. Secondly, to determine whether there was a correlation between neural and behavioural outcomes such that increases PFC activation may be associated with better performance, or vice versa, in older adults. In doing so, this may reveal how older adults mitigate their attention capacity through prefrontal executive involvement or adopt compensatory neural strategies to meet the demands of difficult dual-tasks.
4.1 Neural
According to our initial hypothesis, ∆HbO2 was expected to increase from single- to dual-tasks based on the principles of STAC-r [5]. This prediction was based on the neuroimaging literature which suggests that older adults exhibit more widespread and bilateral activation in the PFC during dual- versus single-tasks and, therefore, greater dependency on executive control compared to younger adults [1, 3]. Contrary to this expectation, this study demonstrated a significant decrease in ∆HbO2 and ∆HbR between walking alone (i.e., single-task) and walking with a cognitive task (i.e., dual-task). These findings are in line with several reports that observed a decrease of prefrontal cerebral oxygenation and an alternative strategy to mitigate the demands of dual-task walking [18, 45]. One possibility is an automatic locomotor control strategy which would be beneficial in dual-task situations to minimize interference with other controlled processes [11, 46]. The PFC’s contributions to walking include managing the attentional demands and motor planning associated with safe and efficient displacement [11, 15]. However, executive resources are limited and may be reorganized depending on task demands. Studies have shown that decreased PFC activation is associated with automatically controlled tasks and walking, in particular, is amenable to automation because it is well learned [47, 48]. Therefore, increased prefrontal activation may only be observed in individuals who show a loss of automaticity such as in people with neurological disorders or frail older adults [8, 14, 29, 49]. Based on the data presented in Table 2, the older adults in this study demonstrated high scores in cognitive function, walk speed (i.e., > 1 m/s) and no frailty, amongst other factors, which are typically associated with decreased executive functioning. These measures suggest that our participant group was high functioning and could rely on an automatic locomotor strategy to free up cognitive resources in the PFC.
Table 2
Mean neuropsychological and health status test scores (Mean ± SD).
Test | n = 20 |
MoCA (/30) | 27.2 ± 1.2 |
Digit Forward (score/16) | 10.7 ± 1.6 |
Digit Backward (score/14) | 7.3 ± 1.9 |
Digit Symbol Substitution test (# of symbols /93) | 45.0 ± 9.7 |
TMT A (s) | 37.9 ± 12.7 |
TMT B (s) | 83.3 ± 25.6 |
SPPB (/12) | 11.1 ± 1.6 |
FES-I (/64) | 20.8 ± 3.6 |
GDS (/30) | 3.2 ± 3.0 |
Participants were also asked to subjectively rate how much attention they paid towards the cognitive versus walking task. Their responses reflected an automatic control strategy in that they reported focusing < 39% on walking during all the cognitive tasks. The cognitive tasks may have also served as an external focus which has been known to facilitate automatic processing [10, 12]. This has been outlined in the “constrained action hypothesis” which suggest that focusing on the outcome of a movement (i.e., external focus), rather than the movement itself (i.e., internal focus), minimizes interference with other consciously controlled tasks [50, 51]. Similarly, diverting attention away from a postural task (i.e., to a cognitive task) even when cognitive demands are low may provide an external focus to improve motor performance [52]. As such, compared to walking alone, responding to the various stimuli during the dual-tasks may have helped draw attention away from walking and allowed for greater stability without greater recruitment of the PFC. Conversely, in the absence of a cognitive task, attention could be drawn to both internal and external sources thereby engaging greater executive control.
Healthy individuals inherently shift between automatic and executive control strategies to mitigate cognitive demands [11, 15]. However, studies have also demonstrated age-related decreases in cerebral blood flow (CBF) to the PFC due to changes in brain structure [53]. The reorganization of locomotor control pathways and a reduction of CBF with age may, therefore, contribute to an overall reduced availability of prefrontal oxygenation. Dietrich’s [54] theory of hypofrontality suggests that there is a redistribution of metabolic resources from prefrontal brain regions to motor regions during tasks such as walking due to the complex integration of sensory, motor and autonomic processes. In other words, the brain is limited by a finite supply of metabolic resources that must be strategically allocated based on the most critical demands [54]. Taken together with automaticity, hypofrontality may cause a downregulation of metabolic resources in the PFC which can be redistributed to other brain regions to supplement motor control. Regions outside the PFC could not be measured within the scope of this study, however, studies have shown heightened brain activation in motor areas such as the premotor [55] and supplemental motor area [55–57] during dual-task walking. These brain regions should be further examined simultaneously with the PFC to determine whether a decrease in prefrontal cerebral oxygenation from single- to dual-task corresponds with changes in motor regions when walking more automatically.
We must also acknowledge certain study parameters including the (i) cognitive and (ii) motor tasks that differentiate this study from others in the literature. (i) Cognitive tasks: Verbal fluency [13, 19, 20] and counting backwards [21, 25] are the most commonly used tasks in dual-task studies that demonstrate increased or no change in cerebral oxygenation between single- and dual-tasks [18]. Our study used processing speed, neural inhibition and working memory tasks which continuously prompted responses and engaged participants based on a random sequence of stimuli. This differs from verbal fluency and counting tasks in that participants were not provided with a starting cue (i.e., a letter or number) after which they could respond at their own pace. The external focus of the cognitive tasks and unpredictable pattern of stimuli may have helped recruit automatic control pathways by ensuring that the full duration of the task was attention-demanding [10, 58]. (ii) Motor task: Walking trajectories vary significantly across studies due to equipment and space constraints. As evidenced by studies examining obstacle negotiation, the interruption of steady state walking caused increased PFC activation and may equally impede automaticity [8, 19, 29]. Our study provided participants with a 10 m pathway to maximize straight-line walking which is considerably longer than studies examining gait along electronic walkways [3, 20, 21, 59]. Therefore, our walking task provided longer stretches of steady state walking and a greater opportunity to automatize gait than studies using shorter walkways.
Lastly, in addition to the ΔHbO2 decrease, there was also a decrease in ΔHbR between the single- and dual-tasks. ΔHbR is a reliable measure of neural activation but is less commonly reported in the literature. This is due to its low signal amplitude making significant changes between baseline and task conditions more difficult to obtain [60]. The low signal amplitude also means that HbR is less likely to be contaminated with physiological artifacts and also results in a lower signal to noise ratio [60]. As such, capturing a significant HbR change that mirrors the HbO2 findings further supports a decrease in brain activation between single- and dual-tasks.
4.2 Behavioural
Examining gait speed in older adults alongside behavioural measures such as response time and accuracy may offer insights into the cognitive-motor interactions underlying dual-task walking. Gait speed changes in older adults have been well documented in the literature such that increasing attentional demands while walking may affect walking performance [15, 27, 28]. Findings from the present study partially support this in that gait speed decreased but only during the most difficult cognitive task. Gait speed maintenance across the first three levels of task difficulty may be explained by an automatic locomotor control strategy, as described in the neural findings. However, this strategy may not have been sufficient to mitigate the demands of the DNS dual-task. As suggested in the “posture first hypothesis,” older adults subconsciously prioritize gait over cognitive performance to ensure safe ambulation [8, 9, 61]. Slowing gait speed may, therefore, be a combination of prioritization and compensation strategies to ensure older adults can function safely under complex task demands. It is worth noting that older adults commonly decrease their gait speed < 1.0 m/s during dual-tasks which is also a cut-off used to identify individuals who are at a greater risk of falls [20, 28, 62, 63]. When the older adults in this study decreased their gait speed during the most difficult task, it still remained on average > 1.0 m/s. This may further indicate the physical status of the participants which could have an impact on performance as compared to other studies in the literature [13, 64].
Decreased response time and accuracy performance may also be a consequence of gait prioritization. Our findings demonstrated increased response times from the easiest to the most demanding task. More specifically, the response times in the SRT task were significantly faster than the GNG and NBK tasks. However, the GNG and NBK tasks were not significantly different from one another. This was expected in that compared to the SRT task, the GNG and NBK tasks involved more complex processing steps. For example, the simple reaction time task required a response after each stimulus whereas the GNG task forced the older adults to first discriminate between a “go” and “no-go” stimulus before responding [31]. Similarly, the NBK working memory task involved maintaining and updating information before responding to the stimuli [6]. Based on these findings, more complex processing steps require more processing capacity. This was evident during the more difficult tasks as the older adults slowed their response times significantly during the inhibition and the working memory tasks compared to the SRT task. Further, the older adults responded less accurately as the difficulty level increased. However, there were no differences between the working memory tasks. These findings support our difficulty manipulation such that participants were most accurate during the processing speed task and least accurate during the working memory tasks.
In line with the literature, increasing task difficulty was expected to result in lower accuracy [1, 65, 66]. Interestingly, participants maintained their accuracy > 80% throughout all the dual-tasks. This suggests that a high level of performance is achievable with increasing cognitive demands when cognitive resources are allocated effectively. However, participants were less accurate during the dual- versus single-tasks. This has been demonstrated in the literature whereby participants make more errors during dual-tasks due to the competing demands of performing two tasks simultaneously [65, 67].
4.3 Correlation between cerebral oxygenation and behaviour
There were no significant correlations between the changes in cerebral oxygenation and behavioural performance. More specifically, the changes in cerebral oxygenation across task and difficulty were not associated with gait speed, response time or accuracy performance. This could be due to the small sample of older adults in this study. However, interpreting neural and behavioural findings together revealed that the redistribution of metabolic resources in the PFC may have contributed to insignificant differences in gait speed across the first three levels of task difficulty. The same cannot be said for response time and accuracy performance in which decreased cerebral oxygenation in the PFC did not result in behavioural gains. Future studies should examine automaticity and neural efficiency across task difficulty in regions outside the PFC as certain regions of interest may increase or decrease activity with the maintenance and decline of different performance measures. Follow-up studies should be conducted to determine how this impacts cognition in the long-term. This may equally reveal whether individuals exhibiting decrements in behaviour due to neural inefficiency may be at a greater risk of cognitive decline.
4.4 Limitations
Gait parameters were only quantified using gait speed. Gait speed is commonly used in the literature because it is easily collected in clinical settings, it requires minimal equipment and is a good indicator of motor performance in older adults [13]. However, other measures that capture gait variability including stride length or stride time could complement gait speed measures and may provide greater insight into subtle changes in dual-task performances, different age groups, and different clinical populations. In addition, the choice of fNIRS device limited our data acquisition to the PFC (Artinis, The Netherlands). This device facilitated setup and caused minimal discomfort for the participants, however, we can only speculate as to which other brain regions were involved in dual-tasking and the potential executive-automatic processing shift in walking with increasing difficulty. Despite this, fNIRS has a high temporal resolution compared to other techniques such as fMRI and is a reliable tool for measuring cerebral oxygenation in the PFC [23].