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. 2017 Nov 23;24(1):58–63. doi: 10.1111/cns.12779

No effect of transcranial direct current stimulation of the dorsolateral prefrontal cortex on short‐term memory

Jing Wang 1, Jian‐Bing Wen 2, Xiao‐Li Li 2,✉
PMCID: PMC6489729  PMID: 29171169

Summary

Introduction

Short‐term memory refers to the capacity for holding information in mind for a short period of time with conscious memorization. It is an important ability for daily life and is impaired in several neurological and psychiatric disorders. Anodal transcranial direct current stimulation (tDCS) applied to the dorsolateral prefrontal cortex (DLPFC) was reported to enhance the capability of short‐term memory in healthy subjects. However, results were not consistent and what is the possible impact factor is not known. One important factor that may significantly influence the effect of tDCS is the timing of tDCS administration.

Aims

In order to explore whether tDCS impact short‐term memory and the optimal timing of tDCS administration, we applied anodal tDCS to the left DLPFC to explore the modulatory effect of online and off‐line tDCS on digit span as well as visual short‐term memory performance in healthy subjects.

Results

Results showed tDCS of the left DLPFC did not influence intentional digit span memory performance, whether before the task or during the task. In addition, tDCS of the DLPFC administered before the task showed no effect on visual short‐term memory, while there was a trend of increase in false alarm when tDCS of the DLPFC administered during the task.

Conclusions

These results did not provide evidence for the enhancement of short‐term memory by tDCS of the left DLPFC in healthy subjects, but it suggested an importance of administration time for visual short‐term memory. Further studies are required to taking into account the baseline performance of subjects and time‐dependence feature of tDCS.

Keywords: dorsolateral prefrontal cortex, short‐term memory, transcranial direct current stimulation

1. INTRODUCTION

Processing and storing external information is an important ability for humans during daily activities. One kind of learning and memorizing information is intentional memory, in which knowledge is learned with intentional and conscious memorization, that is, when people are asked to memorize items during memory encoding. The capacity for holding information in mind for a short period of time refers to short‐term memory. Memory span and visual short‐term memory task were usually used to measure the capability of short‐term memory. Poor recognition performance in short‐term memory has been observed in elderly people and in patients with neurological and psychiatric disorders1, 2, 3 such as Alzheimer's disease, Parkinson's disease, and mild cognitive impairment.

Transcranial direct current stimulation (tDCS), a noninvasive brain stimulation method, has been shown to modulate various cognitive behaviors by manipulating the activity of the cortex4, 5, 6 and change the activity of a target brain area. Intentional memory tasks have been demonstrated to be processed in the dorsolateral prefrontal cortex (DLPFC), which has the functions of manipulation and utilization of information.7, 8 Many of these studies have found the effects of tDCS on short‐term memory enhancement in healthy subjects and have consistently found positive effects of anodal tDCS to the left DLPFC.9, 10, 11, 12, 13 While other studies found no effect of anodal tDCS on short‐term memory such as digit span and n‐back tasks.14, 15, 16, 17 Thus, it deserves further exploration for the possible impact factors.

One important factor that may significantly influence the effect of tDCS is the timing of tDCS administration. Previous results showed that administration of tDCS before tasks (“off‐line effect of tDCS”) or during tasks (“online effect of tDCS”) has different or even opposite effects on behavioral output. For example, the combination of anodal tDCS and cognitive task has the opposite effect on motor‐evoked potentials when compared with anodal tDCS alone.18 Thus, we tested memory performance after both off‐line and online tDCS.

In this study, in order to explore whether tDCS impact short‐term memory and the optimal timing of tDCS administration, we investigated whether online and off‐line administration of anodal tDCS applied to the left DLPFC has an impact on digit span as well as visual short‐term memory performance.

2. MATERIALS AND METHODS

2.1. Subjects

A total of twenty‐three healthy right‐handed subjects participated in the study. Thirteen subjects (mean age of 22.7 ± 1.8 years, 5 females) participated in the off‐line experiment. Eight subjects participated in the online experiment (mean age of 22.3 ± 1.9, 4 females). All participants had no metal implantations in their bodies and were medication‐free during the experiments. They had no history of epilepsy or psychiatric disease. All participants gave their written informed consent in accordance with the principles of the Declaration of Helsinki. Subjects were blind to the purpose of the research. This experiment was approved by the Ethics Committee of Beijing Normal University, China.

2.2. Digit span test

Working memory of subjects was tested by the digit span test. It contains two subtasks. One is the digit span forward (DSF) task, and the other is the digit span backward (DSB) task. In the DSF task, a sequence of digits appears on the screen in front of the subjects at a speed of one digit per second. Subjects were asked to remember the sequence and recall it by inputting with the keyboard. The load of a subject's working memory was estimated by the length of sequences which could be correctly recalled. If the recall is correct, the length of sequence increases one digit. If the recall is wrong, the task ended at that level of difficulty. In the DSB task, subjects were asked to recall the sequence in backward order. The initial sequence length was two. The numbers were selected randomly, but identical consecutive numbers were avoided. The maximum length of sequence that subjects could memorize correctly was considered the limit of working memory.

2.3. Visual short‐term memory

Subjects were asked to perform an object‐match task during the encoding stage. Twenty‐five pictures of objects used in daily life were arranged as a 5 × 5 matrix and shown on the screen of the computer. The picture in the middle of the matrix is the same as one of the other 24 pictures. The subjects were asked to click on the picture that exactly matches the middle picture as fast as possible. After each click, the middle picture changed randomly to another picture. After the subject finished this task, 50 Chinese words appeared on the screen. They consist of the names of the 25 objects shown in the previous task as well as the names of 25 new objects. Subjects were asked to recall which objects appeared in the previous task by clicking on the corresponding names. The number of correctly memorized items (HIT) and the number of new items incorrectly memorized as old (false alarm, FA) were recorded.

2.4. Transcranial direct current stimulation

Direct current stimulation was delivered by a battery‐driven, constant‐current stimulator (DC‐STIMULATOR, NeuroConn GmbH, Ilmenau, Germany). Similar to previous research,19 a pair of rubber electrodes covered by saline‐soaked sponges (7 × 5 = 35 cm2) connected the head and the stimulator. For anodal stimulation of the DLPFC, the anodal electrode was placed on F3, according to the international 10‐20 system for Electroencephalography (EEG) electrode placement, which has been validated for DLPFC by a previous neuronavigational study.20 The cathodal electrode was placed at the right supraorbital area. As 2 mA was shown to be an effective intensity for improving working memory,17 current intensity was set to 2 mA. Because the effects of anodal stimulation are time‐dependent, two kinds of stimulation were selected. Stimulation duration was either 10 minutes or 20 minutes (including 15 s ramped up and 15 s ramped down) for the anodal stimulation condition and 30 s for the sham stimulation condition.

2.5. Experimental procedure

We performed two separate experiments. One is the off‐line experiment. The other is the online experiment. Both of the experiments were randomized, sham‐controlled, and double‐blinded.

For the off‐line tDCS experiment, each subject received three tDCS stimulation sessions, namely sham tDCS, 10 minutes of anodal tDCS, and 20 minutes of anodal tDCS. In each session, subjects performed the digit span tests and visual short‐term memory task before and after stimulation. The three sessions were separated by 7 days, and the orders of sessions were balanced. As the baseline of the first session of visual short‐term memory was a surprising incidental memory task, the data from the first session were removed. Data only from the second and third session were collected as short‐term memory performance.

For the online tDCS experiment, each subject received two tDCS stimulation sessions, namely sham tDCS and 20 minutes of anodal tDCS. In each session, subject performed the digit span tests and visual short‐term memory tests before tDCS as baseline. After that, tDCS was administrated for the first 15 minutes while the subject was quiet and for the last 5 minutes while the subject performs the digit span tests and the incidental memory tasks. A diagram summarizing the experiment is shown in Figure 1.

Figure 1.

Figure 1

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Experimental procedures. The tDCS of the DLPFC were applied in either off‐line or online experiment. For the online experiment, the tasks were performed during the last 5 mins of tDCS stimulation

2.6. Statistical analysis

One‐way repeated analysis of variance (ANOVA), with group as the independent variable, was used to compare the differences among the three conditions for the digit span test. As the data from first session were removed, one‐way ANOVA was used for short‐term memory. Tukey's post hoc analysis was used if the ANOVA findings were significant. In the online experiment, t test or Mann‐Whitney U test was used. The significance level was set at α=0.05.

3. RESULTS

3.1. The off‐line effect of tDCS on short‐term memory

For the digit span task, the modulation of tDCS on digit span was measured as the difference of digit span before and after stimulation. In the digit span forward task, the modulatory effect of sham tDCS, 10 minutes tDCS and 20 minutes tDCS were compared. As shown in Figure 2A, there were no significant differences among these three tDCS conditions (F (2,38) = 0.08, P = 0.93), indicating that the modulatory effect of anodal tDCS on the DLPFC for digit forward span was the same as that of sham tDCS. Similarly, results show no significant difference of digit span in the backward task across the three conditions (Figure 2B; F (2,38) = 0.04, P = 0.97). These findings indicate that neither 20 minutes nor 10 minutes of anodal direct current stimulation on the DLPFC change working memory ability.

Figure 2.

Figure 2

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Off‐line effects of tDCS on digit span tasks. (A) Changes in digit span forward score before tDCS and after anodal tDCS of DLPFC. (B) Changes in digit span backward score

For the visual short‐term memory task, tDCS of DLPFC did not show off‐line modulatory effect. As shown in Figure 3A, there was no significant difference for HIT among three stimulation conditions (F (2,19) = 0.94, P = 0.41). Similarly, Figure 3B showed no significant changes for FA (F (2,19) = 1.72, P = 0.21). The change in HIT minus FA shows no difference though the trend of increase (F (2,19) = 1.30, P = 0.3).

Figure 3.

Figure 3

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Off‐line effects of tDCS on visual short‐term memory. (A) Changes in HIT rate (the number of items correctly memorized) before tDCS and after anodal tDCS of the left DLPFC. (B) Changes in false alarm rate (FA, the number of new items recognized as old). (C) Changes in HIT minus FA

3.2. The online effect of tDCS on short‐term memory tasks

We further investigated whether administering tDCS during tasks had similar effects as administering tDCS during rest. In this experiment, we only used 20 minutes of tDCS in the online experiment. We calculated the change in task performance before tDCS and during tDCS.

As shown in Figure 4, compared with sham tDCS, 20 minutes tDCS during the task did not improve either the digit forward score (t (1,7) = 0.22, P = 0.84) or the digit backward score (t (1,7) = 0.18, P = 0.86).

Figure 4.

Figure 4

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The online effects of tDCS on digit span tasks. (A) Changes in digit span forward score before tDCS and during anodal tDCS of DLPFC. (B) Changes in digit span backward score

The online effects of tDCS on visual short‐term memory were shown in Figure 5. HIT showed no significant difference between sham and anodal tDCS (t (1,6) = 0.46, P = 0. 6) (Figure 5A). However, 20 minutes tDCS during the task showed a trend of increase for the FA (Mann‐Whitney U = 1.5, P = 0.06) (Figure 5B).

Figure 5.

Figure 5

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The online effects of tDCS on short‐term memory. (A) Changes in HIT rate (the number of items correctly memorized) before tDCS and during anodal tDCS of DLPFC. (B) Changes in false alarm rate (FA, the number of new items recognized as old). (C) Changes of HIT minus FA

4. DISCUSSION

We found that neither tDCS administered before the task nor tDCS administered during the task influences the digit span and visual short‐term recognition memory.

In our experiment, we found that neither 10 minutes of anodal tDCS nor 20 minutes anodal tDCS had effects on healthy subjects’ performance in the digit span working memory tasks. This result is consistent with a previous study which demonstrated on effect of tDCS of DLPFC on digit span task.15 Similar results were found in a previous study, where 10 minutes of tDCS did not change the working memory capacity of healthy subjects measured by digit span tasks.21 It was reported that 20 minutes of tDCS on the left DLPFC increased performance on the digit span backward task compared with performance before stimulation; however, there was also a trend of improvement in performance under the sham tDCS condition.12 Accordingly, our findings were in agreement with previous results in that performance in the digit span task was improved for both sham and anodal tDCS stimulation conditions, but anodal tDCS showed no significant difference from sham tDCS. These negative results are in line with findings from a meta‐analysis indicating that the effect size of anodal tDCS of the DLPFC on working memory is not significant.22

There were some findings which showed that tDCS of the DLPFC could improve working memory measured by n‐back tasks.9, 10, 12, 23, 24 The inconsistency from our result could be explained by the difference between digit span tasks and n‐back tasks. Working memory processes include multiple factors such as encoding, maintenance, recall, and recognition. One noticeable distinction between digit span tasks and n‐back tasks is whether they involve or recognition. The digit span tasks require subjects to generate or recall the previous information, whereas subjects recognize items as previously presented in the n‐back task.25 It may be the case that the tDCS of DLPFC enhance working memory to a greater extent when recognition speed but not recall performance is required. However, there were other studies reporting negative even impaired n‐back working memory after anodal tDCS.16, 17 A recent meta‐analysis showed that tDCS causes no improvement in n‐back working memory.22 These findings indicate that our negative results could not only be explained by the difference of tasks. It has been reported that age and baseline performance influence the effect of tDCS, especially, selectively improved older adults and subjects with less baseline performance.26 A possible reason for the absent outcome of tDCS is that subjects in our study were young and high‐level baseline performance. In addition, although the maximum length of digits in our digit span test reaches up to 15 to eliminate the ceiling effect, the nonmodulatory effect cannot rule out the possibility of the ceiling effect.

Contrary to past findings that the outcome of external stimulation was influenced by the state of brain at the time of stimulation onset,27 the effect of tDCS on digit span working memory in our study was not different between online stimulation and off‐line stimulation. This may be related to the measurement and comparison method. We compared the baseline and after performance to measure the net improvement of memory performance, while another study found that the short‐term memory performance was enhanced only during the stimulation but not after stimulation.16 In this case, it is likely that the net changes compared with afterward and baseline performance was not detected in the current research.

The negative results in visual short‐term memory matched our working memory result. There was no improvement in the subsequent recognition memory testing neither 10 minutes nor 20 minutes stimulation. The accuracy of recognition was not improved nor impaired in the off‐line experiment. However, the false alarm showed the trend of increase in the online experiment. It was similar to the previous finding that the number of false alarms was increased by anodal tDCS of DLPFC in encoding stage in recognition memory task.28 This trend of impaired visual short‐term memory was only shown in the online experiment (tDCS is administrated during the task) but not in the off‐line experiment (tDCS was administrated after the task). It suggests additional noise information is added by activation of the left DLPFC during anodal tDCS stimulation, leading to less accurate memories and greater false memory traces. By contrast, off‐line stimulation did not exert such impact on memory. These results indicate the activity‐dependent feature of tDCS. However, some limitations of this study need to be noted. Firstly, the small sample size in this task may be insufficient to detect changes. Secondly, because the surprising recognition performance in the first session was removed, the statistic power was limited by the dataset.

5. CONCLUSIONS

In conclusion, our results did not support the anodal tDCS of left DLPFC produces improvements in digit span working memory and visual short‐term recognition memory in young healthy subjects. Nonetheless, the current informative results indicate the need for taking into account the baseline performance of subjects and time‐dependence feature of tDCS to optimize tDCS parameters for improving short‐term memory.

CONFLICT OF INTEREST

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

ACKNOWLEDGMENTS

Authors thank Dr. Zheng Li for editorial assistance. This research was supported by the National Natural Science Foundation of China (No.61273063, No. 81230023, and No. 81701099), Youth 16 Project of Beijing Municipal Natural Science Foundation (7154818), and Dr. Wang is also funded by Beijing Municipal Research Fund for Outstanding Young Scholar.

Wang J‐B, Wen J, Li X‐L. No effect of transcranial direct current stimulation of the dorsolateral prefrontal cortex on short‐term memory. CNS Neurosci Ther. 2018;24:58–63. 10.1111/cns.12779

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