Effects of online parietal transcranial electric stimulation on associative memory: a direct comparison between tDCS, theta tACS, and theta-oscillatory tDCS

Abstract

Associative memory (AM) is the ability to remember and retrieve multiple items bound together. Previous studies aiming to modulate AM by various transcranial electric stimulation (tES) techniques were inconclusive, although overall suggestive that tES could be a tool for AM enhancement. However, evidence from a direct comparison between different tES techniques is lacking. Here, in a sham-controlled cross-over experiment, we comparatively assessed the effects of three types of tES—anodal tDCS, theta-band transcranial alternating current stimulation (tACS), and theta-oscillatory tDCS (otDCS), delivered over the left posterior parietal cortex, during a short-term digit-color AM task with cued-recall. The effects were tested in 40 healthy young participants while both oscillatory tES were delivered at a previously determined individual theta frequency (4–8 Hz). All three active stimulations facilitated the overall AM performance, and no differences could be detected between them on direct comparison. However, unlike tDCS, the effects of which appeared to stem mainly from the facilitation of low-memory demand trials, both theta-modulated tACS and otDCS primarily promoted AM in high memory demand trials. Comparable yet differential effects of tDCS, theta tACS, and otDCS could be attributed to differences in their presumed modes of action.

Transcranial Electrical Stimulation for Associative Memory Enhancement: State-of-the-Art from Basic to Clinical Research

“…Specifically, 18 out of 29 studies found positive tES effects on AM, 7 studies presented evidence of tES decreasing AM performance, while 4 studies reported null effects on all AM outcomes. There is no apparent relationship between the AM effects and the type of tES protocol applied, as positive effects were reported following anodal tDCS [ 32 , 33 , 44 , 47 , 49 , 52 , 53 , 57 ], tACS [ 58 , 59 ], otDCS [ 52 , 59 ], HD-tDCS [ 54 ], HD-tACS [ 48 ] and even cathodal tDCS [ 51 ].…”

“…When PPC was targeted, the effects on AM were predominantly positive [ 34 , 39 , 44 , 47 , 49 , 52 , 59 ], with only three studies showing negative [ 35 , 55 ] or null effects [ 31 ]. The effects of frontal stimulation were much more mixed—some experiments showed AM improvement [ 32 , 33 , 37 , 45 , 48 , 50 , 53 ], while others showed null [ 38 , 40 , 41 , 42 , 45 , 51 , 56 ] or negative effects [ 36 , 42 , 43 ].…”

“…That is, AM enhancement was observed when PPC was targeted [ 44 , 47 , 52 ], and there were no effects in the study that applied tES over the premotor area [ 46 ]. Finally, with respect to the outcome measures, the studies that used cued-recall paradigms to measure AM performance showed mostly positive effects [ 32 , 33 , 37 , 44 , 47 , 52 , 53 , 54 , 57 , 58 , 59 ], while AM performance was often unaffected by tES when assessed in associative recognition paradigms [ 32 , 33 , 35 , 36 , 37 , 39 , 40 , 41 , 48 , 50 , 55 , 56 ].…”

“…It could be argued that, even when AM enhancement is achieved, this is conducted mostly via the facilitation of supporting processes such as attention, executive control, or reasoning that are highly dlPFC dependent [ 77 ]. On the other hand, the evidence suggests that delivering tES to the temporoparietal or posterior-parietal cortex via different tES protocols can facilitate AM [ 34 , 39 , 44 , 47 , 49 , 52 , 59 ] in a persistent and function-specific manner [ 44 , 52 ], even in aging samples [ 63 , 68 ] and persons with Alzheimer’s dementia [ 72 ]. This is in line with previous neuropsychological and neuroimaging evidence on the role of the parietal cortex, specifically PPC in memory [ 78 , 79 ] and in keeping up with the TMS experiments showing the functional relevance of PPC-hippocampal relay for AM [ 80 , 81 , 82 , 83 ].…”

Closed-Loop tACS Delivered during Slow-Wave Sleep Reduces Retroactive Interference on a Paired-Associates Learning Task

“…The difference is that tDCS does not change polarity (i.e., is either positive or negative), whereas tACS rhythmically shifts polarity, which influences the depolarization and hyperpolarization states of the affected neurons. The studies of [ 33 , 37 ] suggested that the phase at which tACS is applied is crucial. Closed-loop transcranial alternating current stimulation (CL-tACS), a technique that involves using feedback from the brain to inform stimulation parameters without online human intervention, provides the most optimized method for delivering stimulation and entraining neurons in the human brain and has only recently been demonstrated [ 38 ].…”