A Novel Perspective on the Proactive and Reactive Controls of Executive Function in Chronic Stroke Patients

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A Novel Perspective on the Proactive and Reactive Controls of Executive Function in Chronic Stroke Patients

 

Qiuhua Yu¹, Xiaomin Huang^1,2, Baofeng Zhang¹, Zhicheng Li¹, Tao Zhang¹, Ziwei Hu^1,3, Minghui Ding¹, Zhenwen Liang^4* and Wai Leung Ambrose Lo^1,5*

• ¹Department of Rehabilitation Medicine, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China
• ²Department of Rehabilitation Medicine, Zhujiang Hospital, Southern Medical University, Guangzhou, China
• ³School of Rehabilitation Medicine, Gannan Medical University, Ganzhou, China
• ⁴Department of Rehabilitation Medicine, The First Affiliated Hospital of Jinan University, Guangzhou, China
• ⁵Guangdong Engineering and Technology Research Centre for Rehabilitation Medicine and Translation, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China

Objectives: To investigate the proactive and reactive control process when executing a complex task in patients with stroke. Proactive control is the preparatory process before the target stimulus, whereas reactive control is an imperative resolution of interference after the target stimulus.

Methods: In total, 17 patients with chronic stroke and 17 healthy individuals were recruited. The proactive and reactive control of executive function was assessed by the task-switching paradigm and the AX version of the Continuous Performance Task (AX-CPT). The general executive function was assessed by Color Trial Test (CTT) and Stroop Test. The behavioral data of the task-switching paradigm were analyzed by a three-way repeated-measures ANOVA, and the AX-CPT data were analyzed by two-way repeated-measures ANOVA.

Results: For efficiency scores in the task-switching paradigm, trial (repeat vs. switch) × group (stroke or control group) interaction effect was significant. Post-hoc analysis on trial × group effect showed a significant between-trial difference in accuracy rates in the repeat trial in the control group regardless of 100 or 50% validity. For the AX-CPT, the main effects of condition and group on response time were statistically significant. The interaction effect of condition (AY or BX) × group (stroke or control group) was also significant. Post-hoc analysis for condition × group indicated that the stroke group had a significantly longer response time in the BX condition than the control group and longer completion time in CTT2 and larger word interference for completion time in the Stroop test than the control cohort.

Conclusions: Post-stroke survivors showed deficits in the performance of proactive control but not in the performance of reactive control. Deficits in proactive control may be related to the impairment of working memory. Interventions that focus on proactive control may result in improved clinical outcomes.

Introduction

Approximately 50–75% of chronic post-stroke survivors have mild-to-moderate cognitive dysfunction (Desmond, Moroney) (1). Executive functions are higher order of cognitive functions that consist of set-shifting, initiation, monitoring one's behavior, and self-regulating functions (2). Basic cognitive functions could be modulated and organized by executive functions to achieve goal-oriented behaviors (3). The research conducted by Laakso et al. (2) showed that ischemic stroke patients aged 55–85 years, who participated in the Helsinki (Finland) Stroke Aging Memory Study (SAM), had worse performance in executive functions assessments than healthy individuals, including the measures of set-shifting, initiation, response inhibition, and strategy formation. Executive function was considered to be the main factor that influenced the clinical outcome and the overall functional status in patients with stroke after rehabilitation (4). This subsequently contributes to limitations in performing daily activities and participating in social activities (2, 5). Therefore, the precise evaluation of executive function capacity in patients with stroke is essential.

The Montreal Cognitive Assessment (MoCA) is commonly adopted as a brief screening test of general cognitive function. Three subtests of the MoCA, which are the Trail Making B task, a phonemic fluency task, and a two-item verbal abstraction task, could be applied to assess executive functions (6). Executive dysfunctions are indicated if the patient could not complete the subtests. There are others specifically designed assessments to evaluate executive functions such as the Stroop test or the Color Trail Test (CTT) (2). A previous study showed that a large sample of stroke or brain tumor patients with lesions in the frontal region performed worse in the Stroop test than healthy individuals. This suggested an inhibition impairment in stroke patients who had unilateral frontal cortex lesions (7). However, the MoCA, Stroop test, and CTT do not consider the patients' capacity in different executive control processes, e.g., after a cue or target stimulus. Braver (2012) proposed the theory of dual mechanisms of control (DMC), which comprised of proactive and reactive controls. Proactive control is an early selection of goal-relevant information that is processed in a sustained manner of the working memory before the occurrence of the cognitively demanding events (8). It plays an important role in orienting the behavior before the event occurs in our daily life. On the contrary, reactive control refers to the immediate resolution of the current conflict or interference (8), especially when the conflict is without any preparation. The DMC model has been employed to explore the performance of executive function in a different sample population. For instance, published literature reported that elderly people and children tended to employ reactive control, while young adults were more reliant on proactive control in the response-compatibility task (9) and in the AX version of Continuous Performance Task (AX-CPT)(10). Thus, the DMC theory provides a better way to understand the flexibility of behavior regulation in complex situations in our daily life (8). However, most of the studies published to date explored executive dysfunctions without investigating the proactive and reactive controls in patients with chronic stroke.

Proactive control impairment is presented as the inability to employ the information conveyed by the cue to prepare for a response to resolve an upcoming conflict, which required working memory and sustain attention (8, 11). Execution of a functional movement requires an extent of motor anticipation (12), which was comparable to that in the proactive control of the DMC model (13). The results of a study that utilized an electroencephalogram to assess motor anticipation in patients with stroke indicated that motor anticipation impairment and hand motor function were moderately associated with motor planning (14). In Delphine et al.'s study, eight stroke patients were required to grasp and hold a brisk loading under predictive and reactive conditions. The onset time of grip force after the impact was significantly later in the paretic hand of stroke patients than in controls during both predictive and reactive conditions (15). The findings of these previous studies suggested that stroke patients have deficit in proactive control in a simple motor reaction task. This deficit may be related to the prominent impairments of motor task initiation and generation with anticipation loss (16). It remains unclear in terms of the behavioral regulation that involves proactive and reactive controls in patients with chronic stroke when executing a complex task that demands executive function.

This cross-sectional study aimed to explore the performance of proactive and reactive controls of executive functions in post-stroke survivors by the task-switching paradigm and AX-CPT. As impairment of working memory, sustained attention, and motor anticipation was previously reported in stroke patients (16–18), the hypothesis of the present study was that proactive control was more affected than reactive control when performing a complex functional task in patients with stroke. The findings of the present study extend the knowledge pool on executive dysfunction in patients with stroke and would be of interest to a wide audience.

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