Clinical assessment scales are notsensitive enough to cognitive dysfunction in high-functioning stroke patients. The dual-task paradigm presents advantages and potential in the assessment and cognitive training of cognitive dysfunction. The study here proposes a dual-task Stroop paradigm to identify cognitive dysfunction in high-functioning stroke patients.
General clinical cognitive assessment scales are not sensitive enough to cognitive impairment in high-functioning stroke patients. The dual-task assessment has advantages for identifying cognitive deficits in high-functioning stroke patients and has been gradually applied in clinical assessment and cognitive training. Moreover, the Stroop paradigm has higher sensitivity and specificity for attentional assessment than conventional clinical cognitive assessment scales. Therefore, this study presents the dual-task assessment based on the Stroop paradigm to identify cognitive deficits in high-functioning stroke patients. This study demonstrates a single- and dual-task evaluation based on the Stroop paradigm and confirms its feasibility through case experiments and synchronized functional near-infrared spectroscopy evaluation. The Stroop reaction time and correct rate are used as the main indicators to evaluate the cognitive level of the subjects. This study protocol aims to provide new ideas to figure out the ceiling effect in general clinical assessment failure for high-functioning stroke patients.
Stroke is the leading cause of disability in humans1 and can cause varying degrees of motor, cognitive, emotional, and other functional deficits2. Some stroke patients with better prognosis and only slight functional defects show greater functional autonomy in daily activities, but the functional state of their disability may not be sufficient to support their return to work or previous activities. These patients are referred to as high-functioning stroke patients3,4. Due to their minor functional deficits, it is hard to identify their dysfunctions, especially in terms of cognitive functions, through the general assessment of function scales, such as the Montreal cognitive assessment (MoCA)5 and clinical dementia rating (CDR)6, which have a ceiling effect and poor sensitivity for identifying mild functional defects in high-functioning stroke patients. Therefore, it is necessary to develop objective and simple methods to identify cognitive dysfunction in high-functioning stroke patients.
In recent years, the advantages of the dual-task paradigm in assessment and training have gradually become valued7,8. For example, patients may perform normally on simple cognitive single tasks (e.g., calculation) but show varying degrees of cognitive decline when additional tasks are added9,10 (e.g., walking while counting). Manaf et al. found that stroke patients often use compensatory strategies when performing cognitive-motor dual tasks, such as maintaining stability by sacrificing cognitive task performance11. Therefore, the dual-task assessment may have advantages in identifying cognitive deficits in patients with high-functioning stroke. On the one hand, the content of the dual-task assessment is closer to daily life than a single task, such as walking while observing the surrounding environment or talking and calling. In previous studies, the walking + naming task and walking + crossing obstacles task were designed to simulate walking in real environments12.
On the other hand, the executive ability in dual tasks has a close relationship with divided attention (belonging to the category of advanced cognitive function)13. Divided attention is the ability to handle multiple tasks simultaneously and allocate attention to two or more tasks14. This cognitive skill is of great significance to improve the efficiency of daily activities. Therefore, the results of the dual-task assessment can be used for reflecting the individual's divided attention. Normally, people can deal with two or more simple tasks simultaneously in their daily lives and are not disturbed. However, when brain function is impaired, there may be more dual-task interference when faced with simple dual tasks; that is, when performing dual tasks, the reduced divided attention may be likely to cause the performance of one or two tasks to be impaired15. It is concluded that dual-task execution is more likely to be able to detect advanced cognitive function impairment in patients with high-functioning stroke.
The Stroop paradigm is a classical experimental paradigm to study the Stroop effect (also known as the conflict effect)16, which has been widely used in attention assessment in cognitive function tests, especially in the field of attention inhibition17. The classical Stroop effect refers to the fact that it is difficult for individuals to respond quickly and accurately to non-dominant stimuli due to the interference of the dominant response. This results in a longer response time and lower response accuracy for non-dominant stimuli. The difference in reaction time or accuracy rate between dominant and non-dominant reactions is the Stroop effect18. Therefore, the Stroop requires high levels of attention19. Smaller Stroop effects represent higher attentional inhibition, while larger Stroop effects represent a decline in attentional inhibition18.
The Stroop paradigm may be more suitable for assessing cognitive dysfunction in patients with high-functioning stroke and has higher sensitivity and specificity for attention assessment than the traditional clinical assessment scale20. Therefore, this study designed a dual-task assessment based on the Stroop paradigm to identify cognitive deficits in high-functioning stroke patients. The protocol also includes clinical assessment of cognitive function, lower limb motor function, and balance function in stroke patients to ensure that patients can complete the dual-task assessment. Functional near-infrared spectroscopy (fNIRS) was used as an objective evaluation tool for brain function to detect the activation of brain function in high-functioning stroke patients under the dual task. The effectiveness and feasibility of the dual-task assessment scheme based on the Stroop paradigm were verified from the perspective of neuroimaging, which provides new aspects for clinical practice.
This project was approved by the Medical Ethics Association of the Fifth Affiliated Hospital of Guangzhou Medical University (No. KY01-2020-08-06) and has been registered at the China Clinical Trial Registration Center (No. ChiCTR2000036514). Informed consent was obtained from patients for using their data in this study.
1. Recruitment
2. Clinical evaluation
3. Stroop task evaluations
4. fNIRS evaluation
5. Data processing and analysis
This study presents results from a high-functioning stroke patient, who was a 71-year-old male who suffered from ischemic stroke with left hemiplegia 2 years ago. The magnetic resonance imaging (MRI) presented bilateral chronic infarction from the basal ganglia to the radiating crown. He was able to walk and live independently in the community but was not satisfied with his cognitive recovery. However, the functional assessments were all within the normal range: FMA = 100, BBS = 56/56, TUGT = 6, MoCA = 26/30, CDR = 0.5, Albert's Test = 0. Moreover, we also recruited one young female healthy subject as the control. The subjects' information is shown in Table 1.
The single/dual-task assessment results based on the Stroop paradigm showed that, in high-functioning stroke patient performing the single-task Stroop test, the RT of the congruence test trials was shorter than that of the incongruence test trials, and the ACC was comparable to the incongruence test trials (RTCongruence = 547.62 ms, RTIncongruence = 565.07 ms; ACCCongruence = ACCIncongruence = 100%). When performing dual-task congruence test trials, the RT of high-functioning stroke patients was higher than that of healthy young subjects, and their ACC was also relatively lower (RTstroke = 587.03 ms, RThealth = 363.07 ms; ACCstroke = 93.33%, ACChealth = 100%), and the difference in the incongruence test trials was greater than that in the congruence test trials (RTstroke = 613.03 ms, RThealth= 384.67 ms; ACCstroke = 90%, ACChealth = 100%; Table 2).
The results for brain function showed that the β value of ROIs in the stroke patient was lower than that in the healthy young subject during the process of performing dual tasks (RDLPFC: βstroke = −0.006, βhealth = 0.1366; LDPFC: βstroke = −0.0196, βhealth = 0.0976). The rest of the brain regions are shown in Figure 2 and Figure 3.
Figure 1: The single/dual-task Stroop paradigm and the fNIRS design. (A) Congruence test trials. (B) Incongruence test trials. (C) The timeline diagram of the single/dual-task Stroop paradigm. Abbreviations:ms = millisecond; s = second; = left; = right. Please click here to view a larger version of this figure.
Figure 2: The β values in ROIs of the dual-task Stroop effect. The β values of ROIs in the stroke patient was lower than that of the healthy young subject during the dual-task Stroop. Abbreviations: ROIs = regions of interest; RDLPFC = right dorsolateral prefrontal cortex; LDPFC = left dorsolateral prefrontal cortex; RPMC = right promoter cortex; LPMC = left promotor cortex; RSM1 = right primary sensory-motor cortex 1; RPMC = right primary sensory-motor cortex. Please click here to view a larger version of this figure.
Figure 3: Blood oxygen concentration in brain regions of the stroke patient and healthy young subject under the dual-task Stroop effect. (A) Blood oxygen concentration in brain regions of the stroke patient under the dual-task Stroop effect. (B) Blood oxygen concentration in brain regions of the healthy young subject under the dual-task Stroop effect. The β values are indicated by color bars. The results of brain function showed that the β value of ROIs in the stroke patient was lower than that in the healthy young subject during dual-task performance. Abbreviations: R-DLPFC = right dorsolateral prefrontal cortex; L-DLPFC = left dorsolateral prefrontal cortex; R-PMC = right promoter cortex; L-PMC = left promotor cortex; R-SMI = right primary sensory-motor cortex; R-PMC = right primary sensory-motor cortex. Please click here to view a larger version of this figure.
Characteristics | Healthy young subject | Stroke patient |
Age (year) | 21 | 71 |
Gender | female | male |
BMI (kg/m2) | 22.27 | 23.81 |
Cognitive assessment | ||
Montreal Cognitive Assessment (MoCA) | 30/30 | 26/30 |
Clinical Dementia Rating (CDR) | 0 | 0.5 |
Albert’s Test | 0 | 0 |
Motor and balance assessment | ||
Brunnstrom stage | NT | V stage |
Fugl-Meyer Assessment (FMA) | 100 | 100 |
Berg Balance Scale (BBS) | 56/56 | 52/56 |
Timed Up and Go Test (TUGT) (s) | 6 | 11 |
Abbreviations: BMI, Body Mass Index; kg/m2, kilogram per square meter; NT, Not testable; s, second. |
Table 1: The baseline information and characteristics of the healthy young subject and the stroke patient.
Congruence test trials | Incongruence test trials | |||
ACC | RT(ms) | ACC | RT(ms) | |
the stroke patient | 93.33% | 587.03 | 90% | 613.03 |
the healthy young subject | 100% | 363.07 | 100% | 384.67 |
Abbreviations: ACC, accuracy; RT, reaction time; ms, millisecond. |
Table 2: The ACC and RT of the healthy young subject and the stroke patient in the dual task. Abbreviations: ACC = accuracy; RT = reaction time; ms = millisecond.
In our study, the results of the routine clinical cognitive assessment scales for the high-functioning stroke patient did not show any significant cognitive deficits. However, these assessment scales might show a ceiling effect and be less sensitive for identifying the mild cognitive deficits of high-functioning stroke patients. Hence, this protocol further selected ACC and RT in dual-task assessment based on the Stroop paradigm as major indicators to identify the cognitive deficits of high-functioning stroke patients. The results showed that, when the high-functioning stroke patient performed the dual-task Stroop paradigm, their RT was significantly longer than that of the healthy young subject, the ACC was also relatively lower, and the difference in the incongruence test trials was greater than that in the congruence test trials. Besides, the study also used fNIRS to detect the subjects' extent of brain activation in cognitive regions during the execution of the single/dual task in real-time so as to verify the feasibility of the scheme. The data show that the β value of ROIs of the high-functioning stroke patient was lower than that of the healthy subject.
This study protocol designed the Stroop paradigm combined with motion control and the motor functional assessment scale modules of the routine clinical scales, including the FMA, BBS, and TUGT. Among them, the FMA was used to assess subjects' lower limb motor function, BBS was used to assess balance function, and TUGT was used to assess the risk of falling. The assessment results were all within the normal range of motor function. The assessment results of the routine clinical scales showed that the stroke patient included in the study was a high-functioning stroke patient. On the other hand, it also ensured that the included subject was capable of completing the motor task in the experiment. In addition, the cognitive functioning assessment scale modules of the routine clinical scales included the MoCA, CDR, and Albert's Test. Among them, the MoCA and CDR were used to assess the level of cognition, and Albert's Test was used to assess whether the subject suffered from unilateral spatial neglect. Considering that the clinical cognitive functioning assessment scales are semi-quantitative and have a ceiling effect and that there is a lack of sensitivity in the assessment of patients with mild cognitive dysfunction, which causes certain limitations in the evaluation of clinical scales for high-functioning stroke patients, a superior approach needs to be found to solve this problem. Moreover, the study protocol used the ACC and RT of the Stroop paradigm as objective indicators to improve the sensitivity of the assessment results.
According to the representative results, when the high-functioning stroke patient performed the single-task Stroop paradigm, the RT of the congruence test trials was shorter than that of the incongruence test trials, and the ACC was comparable between the two test trials. During the single-task paradigm, the high-functioning stroke patient was able to complete the Stroop test well, showing no obvious cognitive deficits. However, when the high-functioning stroke patient performed the dual-task Stroop paradigm, the RT was significantly higher than that of the healthy young subject, and the ACC of the high-functioning stroke patient was lower. Moreover, the difference in the incongruence test trial was more significant than in the congruence test trial. During the dual-task paradigm, the high-functioning stroke patient had a weakened ability to perform both tasks simultaneously due to his potential cognitive deficits. The patient often uses compensatory strategies (i.e., to maintain stability by sacrificing cognitive task performance), which exposes the cognitive deficits in terms of relatively poor task performance. In the incongruence test trials, the difficulty of the cognitive tasks increased, which made the difference in performance between the high-functioning stroke patient and the healthy young subject more significant and more easily exposed the cognitive deficits of the high-functioning stroke patient. Therefore, this study proposes a dual-task assessment approach based on the Stroop paradigm to identify cognitive deficits in high-functioning stroke patients.
In addition, the study also used the fNIRS technique to verify the feasibility of this protocol. In a case study, fNIRS was used to monitor the subjects' brain activation in cognitive regions in real-time during single/dual-task periods, and six ROIs from cognitive areas were selected to calculate the β value30. The results of the case study showed that the β value of ROIs in the stroke patient was lower than that in the healthy subject. In the process of performing the dual task, the healthy subject used brain resources to complete the cognitive task and motor task simultaneously through activating more brain regions; when the high-functioning stroke patient performed the dual task, sufficient brain areas were not active because of partial damage to brain function. Therefore, enough brain resources were not generated to meet the requirements of performing the cognitive and motor tasks at the same time, which made the performance lower than that of the healthy subject. According to the results of fNIRS monitoring, the degree of brain activation in the high-functioning stroke patient was indeed less than that in the healthy subject, which confirmed the feasibility of using the dual-task Stroop paradigm to identify cognitive deficits in high-functioning stroke patients.
Although the number of included subjects is limited in this study, an earlier case study by Zlatko Matjačić et al.31 proved that disturbance balance training using a robot may be a feasible method, and this finding illustrates the effectiveness of the case study shown here. Moreover, this study displays the whole process of the experimental design and demonstrates the feasibility of this protocol with the help of the results of a case study. Before the trial, subjects should understand the rules and perform the processes of the Stroop test sufficiently. Additionally, one to two pretests should be performed by subjects before the formal experiment to make smooth progress and improve the accuracy of the data. Besides, the safety of the high-functioning stroke patient needs to be ensured all the time on the balance ball during the dual-task Stroop paradigm, so one must ensure that there is a professional staff member in charge of the subjects' safety.
This protocol has some limitations. First, this study aims to demonstrate a dual-task assessment method that can identify cognitive deficits in high-functioning stroke patients. The representative results present only one subject's assessment results. Second, this protocol only takes the balance-cognitive task as the dual-task paradigm and fails to show a variety of dual-task assessment schemes. Future studies will be needed to supplement this.
This study proposes the dual-task Stroop paradigm, which could be used to identify cognitive deficits in high-functioning stroke patients.
The authors have nothing to disclose.
This study was supported by grants from the National Natural Science Foundation of China (No. 81804004, 81902281), China Postdoctoral Science Foundation (No. 2018M643207), Shenzhen Municipal Health Commission Project (No. SZBC2018005), Shenzhen Science and Technology Project (No. JCYJ20160428174825490), the General Guidance Program of Guangzhou Municipal Health and Family Planning (No. 20211A010079, 20211A011106), Guangzhou and University Foundation (No. 202102010100), Guangzhou Medical University Foundation (No. PX-66221494), Key Laboratory of Guangdong Higher Education Institutes [Grant Number: 2021KSYS009] and Guangdong Province Department of Education [Grant Number: 2021ZDZX2063].
Balance Ball | Shanghai Fanglian Industrial Co, China | PVC-KXZ-EVA01-2015 | NA |
E-Prime 3.0 | Psychology softwares Tools | commercial stimulus presentation software | |
fNIRS | Hui Chuang, China | NirSmart-500 | NA |