Prefrontal Transcranial Direct Current Stimulation Globally Improves Learning But Does Not Selectively Potentiate The Benefits Of Targeted Memory Reactivation On Awake Memory Consolidation Part 4

4.3. Consolidation of Emotional Memories and Lateralisation of tDCS Polarity

We hypothesized that anodal excitatory stimulation of the right DLPFC (with cathodal inhibitory stimulation of the left DLPFC) would increase the selective enhancement effect of TMR for negative word pairs. 

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However, our results did not confirm a polarity-dependent effect of tDCS for the consolidation of negative items. Therefore, we cannot conclude that the polarity of tDCS applied during a consolidation interval modulates TMR for negative memories. 

Like for a global TMR effect, however, it is possible that the main and powerful effect of tDCS on overall memory performance masked the specific effect of tDCS polarity on the consolidation of negative word pairs. 

Although this possibility should be investigated in further studies, others similarly failed to evidence inter-hemispheric dissociations between left and right DLPFC in the processing of negative emotions, or even obtained unexpected opposite effects. For instance, anodal tDCS over the left DLPFC was found to facilitate the recognition of negative and positive facial expressions (with a more pronounced benefit for positive emotions), while it did not impact the emotional state of the participants [81]. 

Similarly, Penolazzi et al. [82] found that right anodal/left cathodal stimulation over frontotemporal regions facilitated recall for pleasant images, whereas left anodal/right cathodal stimulation improved recall for unpleasant images. 

Notwithstanding, our results should be taken cautiously as neutral word pairs were better encoded than negative ones at the end of learning already. Superior learning for neutral items is surprising given that arousing negative emotional material is usually better encoded [83]. 

Indeed, most studies have investigated the influence of emotional valence in the time course of memory consolidation found emotional memories to be usually better remembered over time [84], probably because the amygdala mediates the organization of memories in the hippocampus and the neocortex [85,86]. In the present study, participants were asked to learn word pairs while listening to an emotionally congruent sound. 

They were not asked to learn the sound. Therefore, the sounds acted as contextual (specific to the word pair) cues rather than elements to be learned. The benefits of TMR on memory recall were expected to be related to the replay of the auditory cues. We speculate here that the weaker encoding of negative associations is related to the fact that the arousing negative sounds acted as contextual cues. 

Indeed, a highly arousing emotional context can impair memory formation processes. For instance, a fMRI study [87] highlighted negative correlations between recall performance and amygdala activation during the encoding of negative word and neutral face pairs, suggesting that amygdala activation induced by negative emotions may disrupt associative memory performance. 

Furthermore, Zhang et al. [88] showed that highly arousing emotional pictures impaired the recognition of neutral words. They found that highly arousing contexts elicited more positive ERPs (as compared to low arousing contexts), suggesting their automatic attentional capture and the presence of cognitive resources engaged to overcome the interference induced by high-arousing context, which would eventually impair learning. 

Thus, it cannot be excluded that the arousing effect of the negative sounds associated with the word pairs was too high, which would have shifted the participants' attention toward the sounds, to the detriment of the associated negative word pairs as compared to the neutral word pairs. Prior studies also found a specific deleterious effect of arousing negative emotions on associative learning [89–91]. 

Such attentional shift might have interfered with encoding and later retrieval processes, possibly masking a specific effect of right anodal/left cathodal stimulation of the DLPFC. In addition to an interference effect due to a high-arousing context, another possible and complementary explanation for a weaker encoding of negative associations relies on the differential effects of negative emotion on item versus associative memory. 

Indeed, it is commonly assumed that negative emotional content enhances memory for the content by boosting amygdala activity, while the binding of items and context subtended by the hippocampal activity might be impaired, resulting in a detrimental effect of negative emotions on associative memory. Guez et al. [90] found that negative emotional arousal had a more pronounced deleterious effect on associative memory in comparison to item memory. 

Similarly, Bisby et al. [91] found a beneficial effect of negative emotion on item memory, whereas it impaired associative memory. Therefore, another explanation for a weaker encoding of negative associative word pairs observed in our study might stem from a dual memory process that differentially triggers an emotional advantage for item memory but a disadvantage for associative memory.

4.4. No Long-Term Benefits of TMR and tDCS

A 30 to 40% forgetting rate was similarly observed in all conditions when retested one week later, suggesting that awake TMR and tDCS-related benefits on memory consolidation are short-lived, contrary to prior reports (e.g., [43–45]). 

The high level of memory performance achieved at the first recall session may have masked the long-term benefit of TMR and tDCS in our study. For instance, in the Flöel et al. study [45], elderly subjects might have had more room for memory improvement, increasing the potential tDCS-related memory improvement in the long term. 

Another possible explanation is that presenting auditory reminders during a period of wakeful rest initially boosts the associated memories but concomitantly puts those into a more labile condition more susceptible to external interference, eventually leading to forgetting. 

For instance, reexposure to a contextual odor while awake was shown to impair the retrieval of image location [29], probably because memories are more labile after reactivation and need to be reconsolidated [70,92], but see [93]. 

Additionally, the time interval between learning and delayed recall was seven days without any reminders. Cueing memories over consecutive days might have led to identifiable benefits in the long term. Further studies are needed to disentangle the temporal effects of both tDCS and TMR techniques.

5. Conclusions

In summary, we have shown in the present study that TMR during a wakeful resting period benefits short-term memory consolidation. However, concomitant tDCS either on right or left DLPFC gave rise to much higher but unspecific memory enhancements, hence abolishing or at least overshadowing the TMR advantage. 

Finally, our results did not evidence a polarity-dependent hemispheric effect of tDCS on the consolidation of emotional negative memories. 

Noticeably, stimulation of the DLPFC during 20 minutes following learning was found to be beneficial for the consolidation of verbal declarative memories. By increasing cortical excitability in prefrontal areas, tDCS might favor the hippocampocortical dialogue subtending memory consolidation processes.

Author Contributions: M.G. was the lead researcher for this study. M.A.N. contributed to the experimental design and the redaction of the article. P.P. contributed to the experimental design, data analysis, and the redaction of the article. All authors have read and agreed to the published version of the manuscript.

Funding: The study was supported by the FRS-FNRS Projet de recherche (PDR) T.0109.13 and the FNRS-FWO Excellence of Science (EOS) MEMODYN project. At the time of the study, Médhi Gilson was FRS-FNRS Research Fellow.

Institutional Review Board Statement: The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Faculty Ethics Committee at the Université Libre de Bruxelles (protocol code 026/2016, date of approval 15 March 2016).

Informed Consent Statement: Written informed consent was obtained from all subjects involved in the study.

Data Availability Statement: Raw data are publicly available at https://osf.io/4a3d5/ (accessed on 27 May 2020).

Acknowledgments: We thank Paolo Bartolomeo for helping with data collection.

Conflicts of Interest: The authors declare no conflict of interest.

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