The objectives of this study were to detect age-related differences in activation of the prefrontal cortex (PFC) during the tasks of hand motions and to determine an activity-related task type activating the PFC. PFC activation during three tasks, three subtests of the Frontal Assessment Battery (FAB), was investigated in 77 healthy adults by using near-infrared spectroscopy (NIRS). The tasks were a motor programming task (FAB 3), a sensitivity-to-interference task (FAB 4) and an inhibitory control task (FAB 5). We divided participants into three age groups of Younger (20 - 39 years), Middle-aged (40 - 59 years), and Older (60 - 81 years), and compared relative changes in oxygenated hemoglobin concentration in the PFC during the tasks. The activation in the frontal pole (FP) and the dorsolateral prefrontal cortex (DLPFC) during a motor programming task and a sensitivity-to-interference task showed no main effects by age. The results indicated that they were not likely to be affected by age-related cognitive decline compared to an inhibitory control task. In addition, in the Older group, a motor programming task induced significantly greater activation than a sensitivi-ty-to-interference task at eleven channels out of twelve on which we focused (<i>p</i> < 0.05). It was suggested that some characteristic factors included in the motor programming task such as repetition of a series of hand motions and attention to action have the potential to contribute to PFC activation in older adults. These findings provide a clue to understanding daily activities available to suppress cognitive decline of older adults by activating the PFC.
In 2015, Alzheimer’s Disease International reported that 46.8 million people worldwide were living with dementia. This number is expected to almost double every 20 years, to 74.7 million in 2030 and 131.5 million in 2050 [
Other studies have reported the effectiveness of training to enhance frontal lobe function: overall frontal lobe function improved in healthy adults in their 20’s to 30’s after specific WM training by using tasks such as the Stroop interference task associated with selective attention, inhibition, and cognitive flexibility, and the span-board task in which the participants were required to recall the location and order of the presented cues [
A recent comprehensive review of the existing literature on behavioral factors suggests that physical activities, cognitive engagement, and leisure activities can decrease the risk of AD or cognitive decline in older adults [
Analysis of the activities actually provided in dementia care such as domestic tasks and handcrafts shows that a person needs to conduct several motions in a repeated and orderly fashion, and select appropriate actions or control behavior in some way in order to perform the activities. They appear to include the process requiring frontal lobe function such as motor programming, sensitivity to interference, and inhibitory control. However, there have been few earlier studies that investigated the impact of such activities on brain function by using the tasks relevant to executive functions of the brain. In addition, although there have been several near-infrared spectroscopy (NIRS) studies using cognitive tests that demand hand motions [
In this study, we selected three subtests of the FAB―FAB 3, FAB 4 and FAB 5―as the tasks to be performed by the participants. People often engage in movements similar to these three tasks in their daily lives. If some of these tasks prove to be effective in promoting PFC activation, the findings will provide important clues to suppression of age-related cognitive decline.
The objectives of this study were to examine whether aging makes any differences in PFC activation during three FAB tasks with hand motions, and to determine what types of task activate the PFC of older adults effectively, as measured by NIRS.
We recruited participants through the University of Hyogo website, and also from the attendees of lectures for the general public held at the university between August and September 2007. Seventy-seven participants were given the Mini-Mental State Examination (MMSE) to check their cognitive function prior to the experiment. MMSE is a screening tool for cognitive impairment, with a maximum possible total score of 30 points and a cut-score of 23 points [
Treitz, Heyder & Daum reported that executive function declines rapidly after age 60 [
This study was conducted in a quiet room at the University of Hyogo in October 2007 (room size: approximately 60 square meters, average temperature: 23.6˚C, average humidity: 63.0%). The participants were instructed to enter the room individually, undergo MMSE, and perform three FAB tasks in a sitting posture with NIRS optodes positioned on the head. A NIRS optode is an optical sensor device to measure the local changes in oxygenated hemoglobin (Oxy-Hb), deoxygenated hemoglobin (Deoxy-Hb) and total hemoglobin (Total-Hb).
The FAB is a standardized measure to assess frontal lobe functions, and consists of six subtests examining conceptualization, mental flexibility, motor programming, sensitivity to interference, inhibitory control, and environmental autonomy. The participants engaged in three tasks selected out of these subtests: a motor programming task (FAB 3), a sensitivity-to-interference task (FAB 4), and an inhibitory control task (FAB 5). These tasks have common characteristics of using WM function and accompanying hand motions to be carried out. A participant performs FAB 3 by imitating and memorizing an instructed series of three hand motions with his/her right hand (fist- edge-palm) on his/her left palm. In FAB 4, a participant taps his/her finger on the desk while recalling given instructions to tap twice when the examiner taps once, and tap once when the examiner taps twice. In FAB 5, a participant is required to tap his/her finger on the desk, or to inhibit tapping while recalling given instructions to tap once when the examiner taps once, and to refrain from tapping when the examiner taps twice. While FAB 4 and FAB 5 are explicit learning tasks, FAB 3 is an implicit learning task that requires continuous attention to a series of hand motions.
Three trials were run for each task, and the order of the three tasks was the same as the standard FAB test. The protocol was as follows: positioning of optodes, instructions for FAB 3 (60 seconds), the baseline period (10 seconds), (FAB 3 [15 seconds] and rest [20 seconds]) × 3 sets, instructions for FAB 4 (60 seconds), the baseline period (10 seconds), (FAB 4 [15 seconds] and rest [20 seconds]) × 3 sets, instructions for FAB 5, the baseline period (10 seconds) and (FAB 5 [15 seconds] and rest [20 seconds]) × 3 sets. During the baseline period and the rest period, we asked participants to gaze blankly at an x-mark on a piece of white paper on the ivory-colored wall in front of them, so they could recover enough to be stable.
NIRS is an effective and noninvasive tool to examine brain activation while performing activities in a sitting posture. Shoyama et al. wrote: NIRS is sensitive to hemodynamic changes at the capillary level, while fMRI (functional magnetic resonance imaging) or BOLD (blood oxygenation level dependent) signals are only sensitive at the small venous vessel level. They suggested that NIRS measurements are more directly correlated to neuronal activities compared with fMRI [
NIRS measures relative changes in the concentration of Oxy-Hb, Deoxy-Hb and Total-Hb. Hoshi, Kobayashi & Tamura noted that HbO2 (Oxy-Hb) is the most sensitive indicator of changes in rCBF (regional cerebral blood flow) in NIRS measurements, and the direction of the change in Deoxy-Hb is determined by changes in both venous oxygenation and blood volume [
The NIRS measurements were performed by means of Hitachi ETG-4000, a 24- channel NIRS system (Hitachi Medical Corporation, Tokyo, Japan) using two wavelengths of near-infrared light (695 nm and 830 nm). Absorption of near-infrared light was measured with a time resolution of 0.1 seconds. Each channel consisted of a pair of optodes―1 emitter (or light source optode) and 1 detector (or detection optode)―and the distance between them was 3.0 cm from each other.
Optodes were positioned on the participant’s forehead according to the International 10 - 20 system, a standard for Electroencephalography (EEG) electrode positioning [
We used virtual registration to ensure that probe channels corresponded to specific brain regions [
DLPFC, the inferior frontal gyrus (including the orbitofrontal cortex), the pars triangularis Broca’s area, and the frontal eye field. We focused on the channels (CHs) reflecting activation of the FP 100% (CHs 2, 5, and 7 in the left hemisphere, and CHs 13, 15, and 18 in the right hemisphere) and the channels which reflect activation of the DLPFC 100% (CH 6 in the left hemisphere, and CHs 19 and 21 in the right hemisphere) or more than 90% (CH 8 [90.5%] and CH 9 [99.1%] in the left hemisphere, and CH 22 [91.9%] in the right hemisphere).
Task performance of FAB 3, FAB 4 and FAB 5 was scored according to the specified criteria of the FAB [
The data were evaluated by the nonparametric Kruskal-Wallis one-way ANOVA with the post-hoc Steel-Dwass multiple comparison tests. Differences in mean Oxy-Hb values among tasks in each group were tested by the nonparametric Friedman repeated-measure ANOVA with the post-hoc Scheffe multiple comparison tests. Age-re- lated differences in mean changes in Oxy-Hb values at each channel among groups were evaluated by the nonparametric Kruskal-Wallis one-way ANOVA with the post- hoc Steel-Dwass multiple comparison tests.
Tasks | Groups | n | Min | Max | Mdn | Q1 | Q3 |
---|---|---|---|---|---|---|---|
FAB 3 | Younger | 28 | 2.00 | 3.00 | 3.00 | 3.00 | 3.00 |
Middle-aged | 26 | 2.00 | 3.00 | 3.00 | 3.00 | 3.00 | |
Older | 23 | 1.00 | 3.00 | 3.00 | 3.00 | 3.00 | |
FAB 4 | Younger | 28 | 2.67 | 3.00 | 3.00 | 3.00 | 3.00 |
Middle-aged | 26 | 2.67 | 3.00 | 3.00 | 3.00 | 3.00 | |
Older | 23 | 2.00 | 3.00 | 3.00 | 3.00 | 3.00 | |
FAB 5 | Younger | 28 | 2.67 | 3.00 | 3.00 | 3.00 | 3.00 |
Middle-aged | 26 | 2.33 | 3.00 | 3.00 | 3.00 | 3.00 | |
Older | 23 | 1.33 | 3.00 | 3.00 | 2.67 | 3.00 |
The perfect score of FAB 3, FAB 4, and FAB 5 is 3.00 points respectively. Mdn = median; Q1 = the first quartile; Q3 = the third quartile.
first quartile and the third quartile were 3.0 points with the only exception of the first quartile of FAB 5 in the Older group (2.67). As a result of the Kruskal-Wallis ANOVA, no main effects of age were detected in FAB 3 (χ2 = 0.153, df = 2, p = 0.927) and FAB 4 (χ2 = 0.531, df = 2, p = 0.767). Whereas, the main effect of age was verified in FAB 5 (χ2 = 9.981, df = 2, p = 0.007). The results of post hoc analysis by Steel-Dwass multiple comparison tests showed that the score of FAB 5 in the Older group was significantly lower than that in the Younger group (t = 2.911, p = 0.010).
The nonparametric Kruskal-Wallis one-way ANOVA showed no main effects of age in FAB 3 and FAB 4 at every channel. However, main effects of age were observed in FAB 5 at CH 2 (χ2 = 8.59, df = 2, p = 0.014), CH 6 (χ2 = 13.23, df = 2, p = 0.001), CH 8 (χ2 = 13.76, df = 2, p = 0.001), and CH 22 (χ2 = 9.74, df = 2, p = 0.008).
At CH 2, significantly greater increase in Oxy-Hb values was observed in the Middle-aged group than the Older group (p = 0.017). The Younger group showed smaller Oxy-Hb values than the Middle-aged group with a p-value of 0.051, which was marginally significant. There was a tendency that activation in the Younger group was small compared to that in the Middle-aged group. The Middle-aged group showed significantly greater increase in Oxy-Hb than the Younger group at CHs 6 and 8 (p < 0.05). The Older group showed significantly greater increase than the Younger group at CHs 6, 8 and 22 (p < 0.05) (
comparison tests of Oxy-Hb mean values among tasks in each group. The upper half of
As the boxplots on the upper half of
Meanwhile, the boxplots on the lower half of
In all groups, FP and DLPFC activation during FAB 3 was significantly greater than or similar to that during FAB 4 and/or FAB 5 (p < 0.05). In other words, FAB 3 activated the FP and the DLPFC of the participants at any age compared to FAB 4 and FAB 5. We speculated that repetition of a sequence of hand motions and attention to action, which are distinctive elements included only in FAB 3, caused such activation.
Three FAB tasks are considered to be the tasks using WM function because participants
FP Area Left Hemisphere Right Hemisphere
perform them retrieving the instructions stored in memory. Rypma, Prabhakaran, Desmond, Glover & Gabrieli described that imaging studies that employ more difficult WM tasks have found results that differ from those of simple retention studies in two important ways [
Bilateral activation observed during FAB 3, FAB 4 and FAB 5 in the this study was considered to indicate that these tasks were such types of “more difficult WM tasks” as Rypma et al. mentioned.
To summarize, three FAB tasks used in this study required bilateral PFC activation to some extent. On the other hand, Dubois et al. reported that the group of healthy adults (mean age 58.0 ± 14.4) scored approximately 18 points, the perfect score of the FAB [
The three age groups in this study showed no significant difference in the scores of FAB 3 and FAB 4, and the main effects of age were not detected at any channels between the Oxy-Hb values during FAB 3 and those during FAB 4.
The results indicate that the motor programing task and the sensitivity-to-interfe- rence task in this study have the potential to activate the FP and the DLPFC regardless of age, although both tasks were simple enough for most adults to perform with few or no errors. On the other hand, the score of FAB 5 in the Older group was significantly lower than that in the Younger group. This indicates that FAB 5 related to inhibitory control is more likely for older adults to make errors compared to younger adults, which is consistent with age decline of the inhibitory control function reported by Hasher et al. [
Age-related differences were also observed in Oxy-Hb values at one channel in the FP area during FAB 5: The Oxy-Hb value at CH 2 of the Middle-aged group was higher than that of the Younger group, while that of the Older group were lower than that of the Middle-aged group (
To perform FAB 5 or an inhibitory control task, middle-aged or older adults aged 40 years or over needed more activation in the left DLPFC and, in addition, older adults aged 60 years or over needed more activation in the right DLPFC than younger adults. On the other hand, activation in the FP in the left hemisphere was lower in older adults over 60 than middle-aged adults.
Insufficient activation in the FP in the left hemisphere appears to have some relation with the degraded performance of FAB 5 in the Older group.
The FAB 3motor programing task has characteristics that activate the FP and the DLPFC more than the other FAB tasks, regardless of participant age. To perform the implicit learning tasks of FAB 3 correctly, a participant must pay continuous attention to a series of hand motions demonstrated by the examiner. In the explicit learning tasks of FAB 4 and FAB 5, a participant must pay attention to the sound of the examiner’s tap. It was reported that the FP and the DLPFC were activated when the participant learned a motor sequence accompanied by finger movements by using a keypad with four keys, and that the left DLPFC was activated when the participant performed the same motor sequence paying attention to the pre-learned motions [
This study indicates that a motor programming task has the potential to activate the FP and the DLPFC compared to a sensitivity-to-interference task and an inhibitory control task in older adults aged 60 years or over.
From the results of FAB 5 in the Older group, the activities including inhibitory control were found to be rather difficult for older adults aged over 60 years to do without errors. Doing such activities would be useful for maintaining the inhibitory control ability of older adults. However, generally speaking, they tend to avoid engaging in activities they cannot do well in their daily lives, because the experience of failure can lead to loss of confidence or low self-esteem. Especially, older adults with declined cognitive function can easily make mistakes. Once they lose confidence, they may give up doing even the activities they are still able to do. Therefore, if the activities are at a level of difficulty that most people can do without failure, older people can easily engage in the activities continuously.
Van Halteren-van Tilborg et al. suggested that AD patients are capable of implicit learning acquired unintentionally by repeated exposure to skills [
It was previously reported that the PFC was only activated during new motor sequence learning for young adults with a mean age of 32.5 years [
This study suggests that doing activities such as housekeeping or gardening frequently and consistently in their daily lives is meaningful in activation of the FP and the DLPFC, and can potentially to help suppress decline of the PFC function in older adults.
In this study, we used a 24-channel NIRS system, which can reflect activation in the DLPFC region, but cannot detect activation in the whole FP. We used the subtests of the standard FAB test as the tasks requiring WM function that appeared to be included in activities in daily living. Further studies will be necessary on PFC activation during practical activities.
PFC activation during three FAB tasks was compared by means of a 24-channel NIRS system among three groups: the Younger group aged 20 - 39 years, the Middle-aged group aged 40 - 59 years, and the Older group aged 60 ? 81 years. It is generally known that PFC activation tends to decline in older adults; however, this study showed that activation in the FP and the DLPFC during a motor programming task and a sensitivity- to-interference task were not likely to be affected by age-related decline compared to an inhibitory control task. In addition, a motor programming task induced greater activation than a sensitivity-to-interference task in the Older group, at eleven channels out of twelve on which we focused. These findings suggest that activities including repetition of a series of simple hand motions accompanied by attention to action have the potential to activate the PFC, and practicing such activities in daily living may be helpful to older adults in suppressing cognitive decline.
This research was supported by funding from Awaji Landscape Planning & Horticulture Academy in 2007. We are grateful to Dr. Shiho Sugihara, Affiliate Associate Professor at the University of Hyogo, and Kuniko Ogihara, horticultural therapist, for experimental support in performing NIRS. In addition, appreciation is extended to Marni Barnes, Affiliate Professor at the University of Hyogo and Dr. Tamaki Amano, at the Graduate School of Medicine, Kyoto University, for providing thought-provoking input.
Toyoda, M., Yokota, Y. and Rodiek, S. (2016) A Motor Programming Task Activates the Prefrontal Cortex More than a Sensitivity-to-Interfe- rence Task or an Inhibitory Control Task in Older Adults. Journal of Behavioral and Brain Science, 6, 433-447. http://dx.doi.org/10.4236/jbbs.2016.611040