2022 Volume 22 Issue 1 Pages 2-6
Episodic memory is a type of declarative memory important for daily activities. A decline in episodic memory is a common characteristic of aging. Recent studies have shown that transcranial electrical stimulation (tES) improves memory function. To maximize these tES effects, it is necessary to determine which stimulation protocols are effective in improving memory function. This study focused on the optimal timing of stimuli in memory processes using tES. The effects of tES on improving verbal episodic memory in neuromodulation were reviewed.
Episodic memory is a type of declarative memory, which refers to the memory of an event in a person’s life [1]. During aging and neurodegenerative diseases, episodic memory decline is an effect of healthy aging on an individual’s changing mental function [2] [3]. Furthermore, the decline in memory associated with aging affects independence and quality of life. Therefore, discovering ways to reduce cognitive decline through memory enhancement can reduce the social and economic burden. Many recent studies have shown that electrical stimulation of the brain can temporarily modulate human memory processing. However, the optimal timing of transcranial stimulation to improve episodic memory remains under discussion.
This review discusses studies on the optimal time for noninvasive brain stimulation to improve verbal episodic memory.
Episodic memory refers to the memory of an event experienced by an individual in the past. Memory encoding, storage, and retrieval are three important aspects of information processing. When the brain receives new information, it quickly encodes and forms weak memory trials. A long consolidation process transforms weak memory markers into long-term memory markers. When code memory is recalled, it becomes unstable and susceptible to interference [4] [5] [6]. Information recall, accurate encoding, and effective extraction are also necessary [2]. The process of restoring memory stability requires reconstruction [7].
Interventions have recently been implemented to increase memory through transcranial electrical stimulation (tES), a noninvasive brain stimulus. Transcranial direct current stimulation (tDCS) is a type of tES that can improve memory. tDCS changes the function of the cortex by constantly applying weak direct currents (usually 1-2 mA) to the scalp. It is considered to modulate the remaining membrane potential of neurons when polarized. Thus, anodal tDCS induces depolarization of resting potential and increases brain excitability. Conversely, cathodal tDCS induces hyperpolarization of the resting potential and suppresses the excitability of the cortex [8] [9] [10].
Recent studies have shown that active tDCS can have long-term effects by reconsolidating memory.
Manenti et al. [11] examined changes in verbal episodic memory in healthy elderly and young participants using anodal tDCS in the dorsolateral prefrontal cortex (DLPFC) or parietal cortex (PARC) compared to sham stimulation. Participants were tasked with memorizing words displayed on the screen during the encoding phase. After an interval, participants were instructed to recognize whether the displayed word was “new” or “old.” tDCS was applied during the recognition phase. Anodal tDCS applied to the DLPFC and PARC in the right and left brains of young adults and to the DLPFC and PARC in the left brain increased memory recognition compared with sham stimulation in older adults. These results suggest that active tDCS during the recognition phase may be an appropriate tool for modulating episodic memory.
Sandrini et al. [12] confirmed the effects of repetitive transcranial magnetic stimulation (rTMS) during the reconsolidation of memory processes. They found that encoding words on day 1 and rTMS of the prefrontal cortex (PFC) on day 2 enhanced verbal episodic memory.
Sandrini et al. [13] also conducted a study of healthy older adults to confirm the improvement in episodic memory by applying anodal tDCS to the left DLPFC. The protocol applied active tDCS on day 2 with the words learned on day 1, and the recognition tasks were performed on days 3 and 30. The words learned were compared on day 2 in three groups: anodal tDCS group with recall, anodal tDCS group without recall, and sham tDCS group. The anodal tDCS group (both with and without reminders) retained more memory after day 30 than the sham group did.
Using a similar protocol, Manenti et al. [14] applied anodal tDCS to the left DLPFC in older participants with subjective memory disorders. They showed that anodal tDCS is better at retaining recognition memory after day 30 than the retention associated with sham stimulation. These systematic results indicated that tDCS could facilitate access to reduced memory traces.
Sandrini et al. [15] studied the effects of tDCS during learning using different protocols. The results showed that active tDCS during learning enhanced episodic memory compared with sham stimuli on day 3. Interestingly, this study showed no enhancement in episodic memory on day 30.
These studies suggest that active tDCS may be a useful tool to improve memory consolidation. However, it is necessary to understand that the facilitation of memory reconsolidation by applying tDCS depends on the stimulus timing during the memory process.
Recent research has shown that neuronal vibrations play an important role in restoring episodic memories [16] [17]. Transcranial alternating current stimulation (tACS) has attracted attention as a new tES [18]. tACS directly modulates the activity of vibrating nerves under the electrode by alternating the current between the two electrodes installed on the head. [18]. It alters brain rhythms, especially when external vibrations are close to the natural frequency of the stimulated cortical region [19]. tACS is increasingly used to regulate memory function and other cognitive abilities [20] [21].
Osipova et al. [22] identified the vibration activity of gamma (60-90 Hz) and theta (4.5-8.5 Hz) during declaration memory operations in healthy participants. Theta and gamma were identified to facilitate memory encoding and retrieval. Oscillatory activity in the gamma band has been identified during memory encoding and retrieval operations.
Javadi et al. [23] used tACS of the left DLPFC in healthy adults to study the effects of oscillatory brain stimulation during coding and retrieval. Frequency concordance was also checked and compared when the same frequency was used for encoding and retrieval (60-60 Hz or 90-90 Hz) and when different frequencies were used (60-90 Hz or 90-60 Hz). The results showed that gamma oscillations in the left PFC generated declaration enhancement of memory when the same frequency (60-60 Hz or 90-90 Hz) was used for encoding and retrieval.
Based on these studies, Nomura et al. [24] tested whether gamma stimulation has a lasting effect on healthy adults at the same frequency for encoding and retrieval in episodic memory tasks. The protocol consisted of applying a 60 Hz gamma stimulus while learning a word (encoding) on day 1 and a 60 Hz gamma stimulus of the same frequency during a recognition task (retrieval) on day 2. On day 7, the recognition task was performed in relation to the sham stimuli. The results showed that gamma stimulation at the same frequency for encoding and retrieval preserved memory recognition on day 7 (Fig. 1).
However, only a few studies have used the tACS. Further trials are needed to clarify the effects of tACS on declarative memory.
In this review, we summarized the enhancement of declarative memory in response to transcranial electrical stimulation. tES is a tool for enhancing brain function during neurorehabilitation.
Thus, tES has the potential to improve declarative memory. It is expected that future tES protocols will be developed to identify the best stimulation to improve memory consolidation.
This work was supported by Grant-in-Aid for Scientific Research (C) 17K01533 and Scientific Research (C) 20K11293 from the Japan Society for the Promotion of Science. The authors would like to thank Editage (www.editage.com) for the English language editing.
