Validation of a brain-computer interface version of the digit symbol substitution test in healthy subjects

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Highlights

  • A novel SSVEP BCI-based DSST was implemented and was test on 12 healthy people.

  • Performance of SSVEP BCI-based DSST was comparable with that of computerized DSST.

  • SSVEP BCI-based DSST was reliable for repeatedly evaluating cognitive function.

  • SSVEP BCI-based DSST can potentially be used for severely motor-impaired individuals.

Abstract

Digit symbol substitution test (DSST), which is a valid and sensitive tool to assess human cognitive dysfunction, has been widely used in clinical neuropsychology. Although several versions of DSST are currently available, most of the existing DSST versions rely on examinees' intact motor function. This limits their utility in severely motor-impaired individuals. A brain-computer interface (BCI) version of DSST was implemented in this study. Steady-state visual evoked potential (SSVEP) was adopted to build the BCI. Nine symbols in the proposed SSVEP BCI-based DSST were designed with clearly different shapes for decreasing measurement errors due to misidentified symbols. To reduce practice effect, furthermore, the digit-symbol pairs of each trial were different. A two-target SSVEP BCI was designed to judge whether the digit-symbol probe in the center of the user interface matched one of the nine digit-symbol pairs above the user interface. All 12 examinees were able to perform the tasks using the proposed SSVEP BCI-based DSST with 96.17 ± 4.18% averaged accuracy, which was comparable with that of computerized DSST. Furthermore, for examinees participating in both offline and online experiment, the accuracies of the online and offline experiments were comparable, supporting that the proposed BCI-DSST was reliable for repeatedly evaluating examinees’ cognitive function over time. These results verified that the proposed SSVEP BCI-based DSST was feasible and effective for healthy subjects.

Introduction

Cognitive impairment is common in various brain diseases, such as schizophrenia, cerebrovascular disease, and major depressive disorder (MDD). These deficits usually decrease quality of daily life and increase additional burden to both patients and society. Therefore, assessing patients’ cognitive function is very important. Currently, information processing speed is one of the most frequently used tests for cognitive impairment assessment and is also a core aspect for neuropsychological testing.

Digit Symbol Substitution Test (DSST) and Symbol Digit Modalities Test (SDMT) have been heavily utilized in measuring switching attention and information processing speed. In the DSST, numbers are presented and examinees are required to fill in symbols that match the numbers according to the 9 digit-symbol pairing information within a limited amount of time. SDMT is essentially the same as DSST, except in reverse; examinees need to match the corresponding number for each symbol when a series of symbols are presented. Although DSST and SDMT involve multiple cognitive processes, containing attention, perceptual/processing speed, visual scanning, and memory, they may be better seen as measuring more general cognition [1]. DSST and SDMT have been shown to be sensitive to cognitive deficit in various neuropsychiatric populations, including schizophrenia [[1], [2], [3]], MDD [4], and Alzheimer's disease (AD) [5]. For example, DSST is a key element for evaluating the cognitive deficit in schizophrenia when compared to the more widely used neuropsychological measures such as word list learning, span tasks, and card sorting [6]. In addition, DSST seems to have better diagnostic value of AD patients from healthy controls than Digit Span and Trail Making task [5].

Currently, multiple versions of DSST are available, such as written, oral, and computerized versions [1,2,7,8]. These versions of DSST have their own advantages. The written DSST using paper and pencil has culture-free design and low literacy requirement. The oral DSST can reduce the dependence on upper limbs, making it possible to measure patients with upper extremity mobility impairments. Recent advances in computer technology make it possible for developing computerized cognitive tests. In computerized cognitive tests, examinees usually need to provide button-press responses and computers can automatically record the behavioral results. Compared with both written and oral versions, the computerized DSST requires less administrative work of examiners and then reduces random measurement error caused by the examiners to some extent. Both written and computerized versions require examinees with intact upper limb function since the two versions need examinees to use the upper limb writing or pressing buttons to finish these tasks. In the oral version the examinee is asked to verbally indicate the answer. Thus, the existing versions of DSST are not suitable for individuals with upper limb dysfunction or non-verbal function. Attention is critical cognitive function in motor skills learning [9]. Moreover, previous study has shown that early deficit of cognitive function can interfere with the intervention effect of motor-impaired patients [10]. Therefore, evaluating cognitive function has a pivotal role in the rehabilitation of motor-impaired patients [11]. To evaluate the cognitive function of severely motor-impaired patients, the present study attempted to develop a novel brain-computer interface (BCI)-based DSST (BCI-DSST). BCI technology can directly connect the human brain with external devices through brain activity. Even though patients with motor impairment cannot send motor commands, they are still capable of sending intent commands by BCIs. Therefore, a BCI-based DSST is a promising method for measuring cognitive function of severely motor-impaired patients.

In this study, a steady-state visual evoked potential (SSVEP) BCI-based DSST was developed. First, nine symbols in the proposed SSVEP BCI-based DSST were designed with clearly different shapes for decreasing measurement errors due to misidentified symbols. Second, the digit-symbol pairs of each trial were different for reducing the practice effect. Third, a two-target SSVEP-based BCI was designed to judge whether the digit-symbol probe in the center of the user interface matched one of the nine digit-symbol pairs above the user interface. Thus, the proposed SSVEP BCI-based DSST can be used for individuals without intact upper limb function. The experiment results of this study verified that the proposed SSVEP BCI-based DSST was feasible and effective for healthy subjects.

Section snippets

Subjects

Twelve healthy and normal vision subjects (6 females and 6 males, aged 19–26 years) participated in this study. All subjects performed two tests. The first test included SDMT, improved version of the SDMT (i-SDMT), computerized version of the DSST (c-DSST), offline BCI experiment, and offline BCI-DSST experiment. The second test contained SDMT, i-SDMT, c-DSST, online BCI experiment, and online BCI-DSST experiment. The time interval between the first and second tests was greater than 1.5 months.

Behavioral performance

Before beginning the offline and online BCI-DSST experiments, the SDMT, i-SDMT, and c-DSST tasks were conducted to measure examinees’ cognitive function. Therefore, we could obtain two behavioral results for each behavioral task. The time interval between the first and second tests was greater than 1.5 months.

Table 1 lists the results of the SDMT, i-SDMT, and c-DSST tasks for the first test. The numbers of correct responses in both the SDMT and i-SDMT tasks (>40) fell within the normal range [20

Discussion

The present study developed a BCI version of the DSST (BCI-DSST) for evaluating cognitive function. The BCI-DSST could automatically record examinees’ responses and then reduced labor cost of examiners. The digit-symbol pairs of each trial were different and the program randomly changed the order of the nine symbols. This design could prevent examinees from memorizing digit-symbol pairs and then reduced practice effects. The proposed SSVEP-based BCI using an FBCCA method allowed examinees to

Conclusion

This study designed and realized a novel BCI-based DSST. A two-target SSVEP-based BCI was developed to send mental commands for replacing button press. The proposed BCI-DSST could be independently completed by examinees and then reduced the examiners’ labor. Online results obtained from twelve healthy examinees indicated that the average accuracy across all examinees was 96.17 ± 4.18%. Furthermore, the accuracy of the BCI-DSST was comparable with that of the c-DSST. These observations verified

Declaration of competing interest

The authors have no relevant conflicts of interest to disclose.

Acknowledgements

Research supported in part by National Key Research and Development Program of China (No. 2017YFB1002505), Strategic Priority Research Program of Chinese Academy of Science (No. XDB32040200), Key Research and Development Program of Guangdong Province (No. 2018B030339001), National Natural Science Foundation of China (No. 61431007 and No. 61603416), Fundamental Research Funds for the Central Universities (No. 3332018191), Western Medicine Guide Project of Guangzhou Health Commission (No.

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    Authors contributed equally to this paper.

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