Theta band high definition transcranial alternating current stimulation, but not transcranial direct current stimulation, improves associative memory performance

Abstract

Associative memory (AM) deficits are common in neurodegenerative disease and novel therapies aimed at improving these faculties are needed. Theta band oscillations within AM networks have been shown to be important for successful memory encoding and modulating these rhythms represents a promising strategy for cognitive enhancement. Transcranial alternating current stimulation (TACS) has been hypothesized to entrain and increase power of endogenous brain rhythms. For this reason, we hypothesized that focal delivery of theta band electrical current, using high-definition TACS, would result in improved AM performance compared to sham stimulation or transcranial direct current stimulation (TDCS). In this pilot study, 60 healthy subjects were randomized to receive high definition TACS, high definition TDCS, or sham stimulation delivered to the right fusiform cortex during encoding of visual associations. Consistent with our hypothesis, improved AM performance was observed in the TACS group, while TDCS had no effect. However, TACS also resulted in improved correct rejection of never seen items, reduced false memory, and reduced forgetting, suggesting the effect may not be specific for AM processes. Overall, this work informs strategies for improving associative memory and suggests alternating current is more effective than direct current stimulation in some contexts.

Figure 1

Trial Overview.

Figure 2

(A) Face and Scene Task (FAST): 27 encoding pairs are displayed sequentially, followed by a distraction task and then the recognition phase. In the recognition phase, 81 pairs are shown in random order with 1/3 consisting of ‘Together’ (Old) Pairs, 1/3 ‘Not-together’ (Lure) Pairs, and 1/3 ‘Never Seen’ (New) Pairs. (B) Memory Outcomes: Five memory outcomes were derived depending on the subjects response.

Figure 3

Study Protocol. Subjects undergo a brief training phase, followed by the complete FAST task to measure baseline performance. Subjects subsequently completed an alternate version of the FAST Task, with stimulation (TACS/TDCS/Sham) applied during the encoding phase. They returned 24 hours later to complete the recognition phase of the recognition test.

Figure 4

High definition Transcranial Electrical Stimulation (HD-TES). (A) Soterix MxN HD-TES system and the HD-Targets software were used to define the optimal electrode montage to focally stimulate the right fusiform cortex. (B) Finite element Modelling based on a normal adult brain template (HD-Targets software) demonstrating a high focality of electric field in the right fusiform cortex (model based on anodal direct current stimulation).

Figure 5

Immediate Memory Performance. TACS is the reference group. (A) Correct Associative Memory: Significant condition*group interaction, with TACS demonstrating improved memory performance compared to TDCS. (B) Incorrect Associative Memory: No difference between groups. (C) False Memory: Significant condition*group interaction, with TACS demonstrating less errors compared to TDCS. (D) Forgetting: Significant condition*group interaction, with TACS demonstrating demonstrating less errors compared to TDCS and compared to Sham. (E) Correct Rejection: Significant condition*group interaction, with TACS demonstrating improved rejection compared to TDCS.

Figure 6

Delayed Memory Performance. TACS is the reference group. (A) Correct Associative Memory. (B) Incorrect Associative Memory. (C) False Memory. (D) Forgetting. (E) Correct Rejection. No statistically signficiant interactions between group and condition at 24 hours.