In the present study, the efficiency of theta/low-beta NFB training improved the participants' episodic and semantic memory. The theta/low-beta PSD of participants in the NFB group significantly increased during training sessions. The participants in the NFB group showed better performance than those in the control group after training, and this effect lasted for one week. The brain activities of the NFB and control groups were different for episodic and semantic memory. NFB group showed higher theta/low-beta than control group during three times recall tests in episodic memory but such higher theta/low-beta only showed on the last day in semantic memory. The different brain activities might imply that the effect of NFB training on semantic memory would appear after one week. These results suggest that theta/low-beta NFB training is effective to improve long-term memory.
We designed the theta/low-beta NFB protocol and introduced auditory stimuli based on previous studies which proposed with visual stimuli12. Additionally, we referred other studies suggested that theta waves may be involved in the consolidation of episodic memory12,23 for our training design. We considered that auditory feedback results in less disturbance than visual stimulation and allows participants to concentrate on appropriately regulating their cognitive control. During the NFB training sessions, the participants followed our instructions and regulated their cognitive process using real-time auditory feedback to improve the theta/low-beta PSD as much as possible. According to our results, the theta/low-beta PSD of participants in the NFB group increased, and the theta PSD were significantly increased during the three-day training sessions. The increments of theta/low-beta PSD and theta PSD did not induce low-beta, beta, alpha, or gamma PSDs during the training sessions. These findings are consistent with the previous study which suggested the specificity of target frequency bands.24 Theta/low-beta protocols can effectively improve episodic memory but low-beta/theta NFB protocols can not be seen the same trend12. The results of the theta/low-beta PSD and theta PSD did not increase over the course of the second stage linearly, similar to previously-reported findings that the brain activities increase unstable during training10,11,25,26,27. We assumed that synaptic consolidation is likely to occur in NFB training, and gaps of several days during training sessions affect neuronal changes28. Despite different timelines, the results of this study are consistent with those of previous studies, suggesting that cognitive control processes are related to theta oscillations29,30 and that the theta oscillations can be trained using theta/low-beta NFB12. Taken together, these results indicate that the theta/low-beta NFB training protocol designed for use in this study to increase theta PSD is effective.
According to our results, the forgetting rate of participants in the NFB group significantly decreased for semantic memory and showed marginal significant in episodic memory after NFB training. In this study, the recall tests were conducted approximately 20 minutes, one day, and six days after memorization. The recall test results for episodic memory obtained 20 minutes after memorization were similar to previously-reported results11,12. The NFB group performed better in the recall tests than the control group at all time points. Although our training protocol required only three days to train the participants, the effects of NFB training remained for one week.
Previous studies have indicated that theta oscillations play an important role in the memory process21,31. Some studies have suggested that the hippocampus theta15 and the increment of the theta band power in the posterior hippocampus32 can be used to predict successful encoding in episodic memory. In this study, our experimental device could only record the brain activities from the surface of the brain; therefore, we could not identify differences in brain activities between the different groups during the encoding task for episodic memory. However, several previous studies have suggested that the increment of theta activity affects episodic retrieval31,33,34. In our study, the theta activities in the NFB group were higher than in the control group during the recall test in the third stage (after NFB training sessions). These results are consistent with those of previous studies12 and suggest that the theta/low-beta NFB training affects subsequent recall tasks of episodic memory for at least one week.
Participants in the NFB group had improved performance for semantic memory after theta/low-beta NFB training. In this study, regression analyses revealed that the difference in memory scores and the difference in theta PSD before and after NFB training were negatively correlated. These differences were not correlated in the control group. This finding was unexpected and suggests that individual theta power, which is related to the sematic processes, was significantly changed after NFB training sessions in the NFB group. This study confirms that theta power is associated with encoding and retrieval in semantic memory. Retrieval of semantic information is commonly seen in language processing. Several studies have shown that theta power supports the process of semantic memory, and that theta power increases during the retrieval of semantic information35,36,37,38,39.
To our knowledge, there are no previous reports of the use of NFB training to improve semantic memory, though several studies have reported improvement of episodic memory after NFB training10,11,12. In this study, we found that both episodic and semantic memory were improved by the theta/low-beta NFB training protocol we designed.
The hippocampus and prefrontal cortex (PFC) play important roles in episodic memory processing40,41. Previous EEG source estimation studies have suggested that frontal midline theta waves are generated by the anterior cingulate and medial PFC42,43,44,45. In addition, other reports have suggested that theta oscillations generated from the PFC in patients with epilepsy can predict the success of coding in episodic memory46,47. Individuals with stronger hippocampus-PFC connectivity can encode pictures into long-term memory better during working memory tasks, suggesting that the relationship between theta activity and memory encoding may depend on the connectivity between the hippocampus and PFC48. In this study, the theta PSD and memory scores were improved after NFB training, indicating that the training protocol used in this study may also affect the deep neural mechanisms including hippocampus and PFC.
The theory of synaptic and systems consolidation includes an important brain circuit that is necessary for transforming short-term memory into longer-term memory28. The transition from short-term to long-term memory is not instant and requires repeated consolidation and other factors (including sleep)28,49,50,51. In this study, we assumed that the mechanism of NFB training sessions included the process of synaptic consolidation. The study design (six sessions of NFB training per day for three days) allows for the enhancement of theta, leading to synaptic consolidation and the translation of the consolidated systems. Therefore, NFB training may not lead to short-term results but lead to long-term consolidation.
The results of the recall test for semantic memory were significantly different compared to those for episodic memory. Several studies have reported that theta/beta NFB protocols modulate the medial frontal areas, which are involved in some cognitive processes including the process of response inhibition22. In addition, the oscillating inhibition model explains the relationship between theta oscillation and retrieval processes that induce forgetting and proposes that theta oscillation inhibits competitive memory52,53,54. The theory of the process of response inhibition and the oscillating inhibition model may explain why the participants in the NFB group achieved better results for the recall test for episodic memory and had higher theta/low-beta amplitudes. The results of semantic memory in the recall test showed a difference with episodic memory, indicating that the mechanisms of these two types of memory are different. The oscillating inhibition model explains why participants in the NFB group had higher theta/low-beta PSD for semantic memory than those in the control group on the final day of the memory period. As test day lag increases, the theta/low-beta PSD increases to inhibit the interference with competing retrieval from target memories as task difficulty increases. The theory of synaptic and systems consolidation proposes that the influence of NFB training on deep neural mechanisms will not be immediately apparent.
Although the episodic and semantic memory were different in terms of memory system or memory recall mode, some interaction between these two types of memory during the memory process via theta oscillations has been reported17,55. In this study, we did not find evidence of a correlation between episodic and semantic memory in the participants’ performances or brain activities. Future studies should focus on understanding how the episodic and semantic memory interacts during memory processing. A new method to differentiate the two types of memory is necessary to understand their independence and interaction.
In this study, participants received only three days of NFB training within one week. We believe that longer training periods would affect the long-term memory more significantly, so we plan to design a longer-term period for the training session in our future works. It had been difficult to encourage the participants to return after a one-month gap between memory tasks. Therefore, this study was designed to include a maximum of one week between the recall test and the encoding task for memory stage. We also plan to design a longer time period experiment for the recall test and encourage participants to come back again after one month, six-month and even one year.
This study explored the trainability of long-term memory and found that NFB training can effectively improve episodic and semantic memory. In addition, we found that the brain activities after NFB training have different performances on the retrieval task in two different types of long-term memory. These results can provide the cornerstone for understanding long-term memory and may be used to treat memory disorders such as patients with epilepsy and theta dysfunction or Alzheimer's disease.