Gamma oscillations modulate working memory recall precision

Abstract

Working memory (WM)-the ability to keep information in mind for short periods of time-is linked to attention and inhibitory abilities, i.e., the capacity to ignore task-irrelevant information. These abilities have been associated with brain oscillations, especially parietal gamma and alpha bands, but it is yet unknown whether these oscillations also modulate attention and inhibitory abilities. To test this, we compared parietal gamma-transcranial alternating current stimulation (tACS) to alpha-tACS and to a non-stimulation condition (Sham) in 51 young participants. Stimulation was coupled with a WM task probing memory-based attention and inhibitory abilities by means of probabilistic retrospective cues, including informative (valid), uninformative (invalid) and neutral. Our results show that relative to alpha and sham stimulation, parietal gamma-tACS significantly increased working memory recall precision. Additional post hoc analyses also revealed strong individual variability before and following stimulation; low-baseline performers showed no significant changes in performance following both gamma and alpha-tACS relative to sham. In contrast, in high-baseline performers gamma- (but not alpha) tACS selectively and significantly improved misbinding-feature errors as well as memory precision, particularly in uninformative (invalid) cues which rely more strongly on attentional abilities. We concluded that parietal gamma oscillations, therefore, modulate working memory recall processes, although baseline performance may further influence the effect of stimulation.

Keywords: Attention; Gamma oscillations; Inhibition; Working memory; tACS.

Fig. 1

The working memory (WM) retro-cueing task and paradigm. a Participants memorized a display of four arrow stimuli differing in orientation and color. Following a delay period, one of the four colored arrows reappeared in a random orientation and participants matched it as closely as possible to the orientation in the original display. In 70% of the trials during the delay, a colored retro-cue was presented highlighting an item that was more likely to be later probed. In these trials, the probe either matched the cued items (validly cued trials, N = 62) or it did not (invalidly cued trials, N = 26). In the remaining 30% of the trials (N = 38), a neutral cue was present during the delay. b Participants performed the working memory retro-cue task in a pre-stimulation session with no tACS (baseline), followed by three experimental sessions at least 48 h apart during which they performed the same WM task while receiving 20 min of bilateral parietal (P3 and P4 on 10–20 EEG system) tAC stimulation at either 10 Hz (α band), 35 Hz (γ band), or Sham. The order of the stimulation conditions was pseudo-randomized across participants

Fig. 2

Current modeling. a Modeling of the electric field induced by 1.5 mA current of the tAC stimulation to the bilateral parietal lobes, which b corresponded to P3 and P4 on the 10–20 EEG system used to locate the target areas. The current modeling performed on ‘ROAST’ (https://www.parralab.org/roast/, Huang et al. 2019) shows a bilateral electric field distribution with maximum current over the posterior parietal areas which we stimulated

Fig. 3

Recall precision during tACS. Changes in recall precision following alpha, gamma-tACS and sham in valid, invalid and neutral retro-cues in the whole sample as well as in low-baseline and high-baseline performers. Each dot indicates a participant’s performance in each condition. Cross symbols refer to the group mean, and asterisks denote significant differences (p < 0.05)

Fig. 4

Probability of target responses (pT) during tACS. Changes in the probability of target responses following alpha, gamma-tACS and Sham in valid, invalid and neutral retro-cues in the whole sample as well as in low-baseline and high-baseline performers. Each dot indicates a participant’s performance in each condition. Cross symbols refer to the group mean, and asterisks denote significant differences (p < 0.05)

Fig. 5

Probability of non-target responses (pNT) during tACS. Changes in the probability of non- target responses following alpha, gamma-tACS and Sham in valid, invalid and neutral retro-cues in the whole sample as well as in low-baseline and high-baseline performers. Each dot indicates a participant’s performance in each condition. Cross symbols refer to the group mean, and asterisks denote significant differences (p < 0.05)