Background
MCI is a transitional stage between normal aging and Alzheimer’s disease [
1]. So far, 16% of people over the age of 70 have been diagnosed with MCI [
2]. And develop Alzheimer’s disease at 4–15% a year [
3]. It is reported that MCI has been identified as an important risk factor for instability and falls in older adults [
4], and the incidence of falls in older adults with MCI is twice as high as that in healthy older adults compared with the older adults with complete cognition [
5].
Both balance control and cognitive function play important roles in preventing falls and injuries in older adults [
6]. MCI is characterized by objective memory impairment over age [
1]. Compared with healthy older adults, the cognitive function of older adults with MCI decreased, including attention, language fluency, and name recall [
7]. At the same time, older adults with MCI showed defects in balance ability and posture control ability [
8], Compared with healthy older adults, there was an increase in postural sway in standing balance control in older adults with MCI, especially a significant decrease in balance in medial-lateral direction [
9]. Balance disorders are positively associated with cognitive impairment, and both increase the risk of falls [
10]. While it is common to perform cognitive tasks while standing or walking in daily life, the ability of older adults with MCI to allocate limited attention resources to posture control decreases, which will lead to a further increase in the risk of falls [
11].
Cognitive-motor control dual-task paradigm is often used to study the interaction between the allocation of brain cognitive resources and neuromuscular behavior control [
12]. According to capacity-sharing theory, cognitive resources are limited in capacity. If the two tasks performed together exceed the available cognitive capacity, then the capacity to perform both tasks optimally will be insufficient, and the performance of either or both tasks will deteriorate [
13]. For example, performing cognitive tasks while standing reduces postural stability, and older adults are more likely to wobble when performing cognitive-postural control dual tasks than performing postural control alone [
14]. Compared with healthy older adults, the older adults with MCI showed higher dual-task costs during level walking, and poor dual-task performance was associated with the transformation of older adults with MCI into dementia, which was an important predictor of future falls [
15]. However, few studies investigate the balance ability under dual tasks in the MCI.
The brain area responsible for executive function is mainly located in the PFC, which is closely related to the dorsolateral PFC [
16]. The relationship between executive function and movement has been extensively studied using the dual-task paradigm [
12]. Cognitive decline associated with executive function may be a contributing factor to postural instability and falls [
17]. A fNIRS study, revealing the compensatory mechanism of PFC activity for standing balance in older adults, found that older adults increased PFC activation compared to young adults during dual-task balance. PFC activation compensates for sensorimotor deficits to maintain stability [
18]. However, at present, there is a lack of research on the relationship between static standing balance and cognitive function in MCI, and there are relatively few reports on the neuroregulatory mechanism of the dual-task paradigm affecting static postural control in MCI.
The present study aims to explore the characteristics and correlation of standing balance control ability and prefrontal oxygenation level in older adults with MCI under single-task and dual-task paradigms compared with healthy older adults. This study might help to understand the neurobiological mechanism of cognition and balance performance and also provide a theoretical basis for the formulation of targeted prevention and clinical rehabilitation intervention strategies. The following hypotheses are formulated: (1) While performing dual tasks, the standing balance control ability of the older adults with MCI was worse than that of the healthy older adults, and also the older adults with MCI required more PFC activation. And (2) the balance ability of healthy older adults and older adults with MCI is positively correlated with the activation level of PFC.
Discussion
This study compared the balance ability and functional brain oxygenation in the PFC among MCI and healthy older adults under single and dual tasks, and also investigated their relationship. Our results partially support the hypothesis that older adults with MCI have poorer balance control than healthy older adults.
The first hypothesis was demonstrated in the present study. Our results showed that under the dual tasks, the balance control ability of the older adults with MCI is significantly lower than that of the healthy older adults. And the PFC activation level of older adults with MCI was higher than that of healthy older adults, which concurred with previous studies investigating the decreased balance control ability in the MCI [
30] and execution of dual-tasks increases PFC activation in older adults with MCI [
31]. Balance control is a complex neuromuscular control process, that involves sensory detection of body movement, integration of sensorimotor information in the central nervous system (CNS), and appropriate programming and execution of neuromuscular responses [
32]. Aging leads to the decline of physical and cognitive function in older adults, and more cognitive resources are needed to perform simple motor tasks in older adults [
33]. However, compared to healthy older adults, the working memory and attention functions of older adults with MCI are impaired [
7], and a decreased integration ability of sensorimotor information during multiple-task postural control [
34]. Therefore, when performing dual tasks, older adults with MCI showed worse balance control than healthy older adults.
Interestingly, we observed that the PFC activation level of older adults with MCI was higher than that of healthy older adults in both single task and dual task
(Table
2). PFC is critical to a person’s ability to selectively allocate attention [
35] and integrate visual and proprioceptive information [
36] to maintain postural stability. Higher PFC activation is usually attributed to a decline in the efficiency of multi-sensory information processing in the aging brain, which leads to automatic impairment of movement, and leads to higher attention demand [
37]. For older adults, PFC activation reflects an attempt to recruit a higher amount of limited neural resources to compensate for sensorimotor deficits to maintain balance control stability [
18]. A previous study consistently found that increased PFC activity could compensate for damaged cortical circuits in other neuropsychiatric disorders to maintain a level of cognitive task performance comparable to that of healthy controls [
38]. In this study, compared with healthy older adults, older adults with MCI have attention deficit [
34] and postural control deficiency [
8]. Structural and functional brain networks in MCI are both disrupted and associated with compromised cognitive performance [
39], and these anatomical and functional changes can interfere with the balance control ability in MCI [
32]. Therefore, older adults with MCI might need more PFC activation to maintain a standing balance.
It is worth noting that there was no task main effect on PFC activation in either two groups. We speculated that the attention resources of older adults with MCI are mainly used for balance maintenance under single task. While our balance control task was relatively simple [
21] and not sufficient to pose a threat to postural control of older adults with MCI. Therefore, older adults with MCI can still handle the low-load tasks without overcompensation and thus do not exhibit over-activation of the PFC [
40]. However, the balance control ability of older adults with MCI decreased in the dual task compared with the single task, the balance control ability of healthy older adults was not significantly disturbed by the dual task. We speculated that when disturbed by the dual-task, neither group of participants increased the activation of the PFC, but the balance control ability of the MCI can not be adequately maintained at the current level of PFC activation, while the healthy older adults can be maintained. This finding may be due to impaired working memory and attention function in older adults with MCI [
7] and reduced ability to integrate sensorimotor information [
34].
The second hypothesis was partially proven as follows: under single task, the balance parameters were correlated negatively with PFC activation parameters in older adults with MCI. That is, the higher the activation level of PFC, the better the balance ability (Fig.
3A). In contrast, the balance parameters were correlated positively with PFC activation parameters in healthy older adults (Fig.
3B). In previous studies, older adults with MCI need more PFC activation to participate in postural control than healthy older adults because of attention deficit [
34] and postural control deficiency [
8]. Therefore, for older adults with MCI, more PFC activation may be more conducive to the maintenance of balance [
41]. As in this study, the better the balance, the higher the PFC activation level in older adults with MCI (Fig.
3A).
A fNIRS study consistently showed that when the level of PFC activation was lower, the performance of the healthy group was better, while that of the MCI group was on the contrary [
42]. In contrast, when healthy older adults performed the single task, the better their balance ability, the lower their PFC activation level (Fig.
3B). We speculate that the differences in brain anatomy and function between the two groups might lead to the opposite results of the correlation analysis. Previous studies have shown that white matter content in older adults with MCI is appreciably different from those in healthy older adults [
20]. And subcortical neuroanatomical changes in MCI, which are a central cholinergic deficit related to the loss of neurons in the nucleus basalis of Mynert and amyloid deposition and neurofibrillary tangles in the mesial temporal structure [
32]. These changes in brain structure and function adversely affect the balance control system in older adults with MCI [
32]. The activation of PFC is to compensate for the subcortical information processing deficiencies in older adults with MCI [
18]. Therefore, older adults with MCI require more PFC activation to maintain a standing balance, that is, the higher the PFC activation, the better the balance.
However, our data shows that the PFC activation parameters of older adults with MCI were positively correlated with the balance parameters under the condition of the dual task, which was opposite to that of older adults with MCI under the condition of the single task (Fig.
3C). None of the balance parameters were significantly correlated with PFC activation parameters in healthy older adults (Fig.
3D). When performing dual tasks, the lower the level of PFC activation in older adults with MCI, the better the balance control ability; this is contrary to the correlation under single task (Fig.
3 A, C). The possible explanation is that there is an interference effect in the dual-task execution of older adults with MCI under the dual tasks, and the simultaneous tasks will interfere with each other, thus affecting the dual-task execution [
43]. This is consistent with the central capacity sharing model [
13]. When attention demand increases, PFC compensatory activities or neural compensation may increase and exceed available resources [
13]. Therefore, when older adults with MCI performe dual tasks, multi-system aging (such as sensory or cognitive impairment, and reduced motor ability) means competition for common neural structures [
44]. Under dual tasks, even if the PFC activation increases, the balance control ability decreases due to the interference of cognitive tasks.
Unlike the MCI, the healthy older adults did not observe the correlation between the PFC activation and balance control ability under the dual task (Fig.
3D). The single task seems to be a relatively simple balance control task for healthy older adults, which may not be challenging enough [
21]. The task priority model [
13] holds that when posture threat increases, older adults give priority to postural control rather than cognitive task performance. Therefore, even if the balance-cognitive dual task is performed at the same time, the interference of the cognitive task is not enough to disturb the balance control, attention resources are prioritized to deal with cognitive tasks. Another possible explanation is that older adults might transfer processing resources to other brain areas under dual tasks [
45]. Since brain activity was measured only in a limited area of the PFC in this study, further study could investigate more brain areas for insight comprehension.
Our findings found that BA45, BA10, and R11 areas play an important role in the standing balance control task of older adults with MCI. BA45 area plays an important role in planning the high-level motion sequences, which not only participates in language processing but also participates in various tasks and content fields [
36]. Previous studies have confirmed that the execution of various cognitive tasks and motor tasks could activate the BA45 area [
46]. We also found that when performing single tasks, older adults with MCI need more activation of the BA45 area to maintain balance and stability. The BA10 area, the largest and most anterior area of the human PFC, is involved in multitasking, especially in selecting and maintaining higher internal objectives while performing other sub-objectives [
47]. Previous studies have shown the functional separation between the medial and lateral surfaces of the BA10 area [
48]. According to “multitasking” tests and functional neuroimaging experiments, the medial surface of the BA10 diverts attention to thoughts guided by sensory stimuli, while the lateral surface focuses on internally generated ideas [
49]. Our study found that there was a significant positive correlation between bilateral BA10 activation and balance control in older adults with MCI when performing dual tasks. We speculated that both the medial and lateral activation of BA10 was evoked simultaneously due to the increase of cognitive task and balance difficulty at the same time, and we required participants to speak out the results of the calculation. The BA11 area is highly susceptible to age-associated changes, including disruption of frontostriatal circuits by diffuse white matter changes and gray matter atrophy [
50]. Previous studies indicate that older adults exhibited significantly greater activation than young adults during motor imagery in R11 [
51]. We also found that older adults with MCI need more activation of the R11 area to maintain balance control during single task.
The current research may be of great significance in strengthen the balance control strategy of older adults with MCI. The theory of brain plasticity holds that the brain can still show plasticity in the face of cognitive decline in old age [
52]. Dual-task training can improve the speed of attention conversion, improve the ability of attention allocation between tasks, and make the allocation of cognitive resources among different tasks more coordinated [
53]. Therefore, our study can be used to guide and formulate targeted task balance control therapy [
53] and optimize alternative interventions such as non-invasive brain stimulation [
52]. Up-regulation or down-regulation of the excitability of specific brain areas (such as BA45 and BA10) of PFC may have a certain effect on promoting balance control in older adults with MCI.
The current study has some limitations. First of all, we only assessed one static standing posture task and one cognitive task for the study, and did not quantify the difficulty level of the cognitive task and balance task. Secondly, this was a cross-sectional study, further studies could focus on the effect of dual-task training on balance and PFC activation in MCI. Finally, due to the limitation of experimental instruments, it is impossible to obtain more information about the cerebral cortex except for PFC.