Dynamic changes in prefrontal cortex involvement during verbal episodic memory formation

Abstract

Highlights We investigated encoding-related post-stimulus brain activity in the prefrontal cortex with repetitive Transcranial Magnetic Stimulation (r-TMS)  We delivered r-TMS during encoding while a word appeared on the screen, and at different points in time after its offset  r-TMS over the ventrolateral prefrontal cortex shortly after stimulus offset decreased subsequent memory accuracy  No effects were found when r-TMS was delivered over the dorsolateral prefrontal cortex at any time point  The involvement of the ventrolateral prefrontal cortex may reflect offset-specific processes. ABSTRACTDuring encoding, the neural activity immediately before or during an event can predict whether that event will be later remembered. The contribution of brain activity immediately after an event to memory formation is however less known. Here, we used repetitive Transcranial Magnetic Stimulation (rTMS) to investigate the temporal dynamics of episodic memory encoding with a focus on post-stimulus time intervals. At encoding, rTMS was applied during the online processing of the word, at its offset, or 100, 200, 300 or 400 ms thereafter. rTMS was delivered to the left ventrolateral (VLPFC) or dorsolateral prefrontal cortex (DLPFC). VLPFC rTMS during the first few hundreds of milliseconds after word offset disrupted subsequent recognition accuracy. We did not observe effects of DLPFC rTMS at any time point. These results suggest that verbal encoding-related VLPFC engagement starts at a relatively late processing stage, and may reflect brain processes related to the offset of the stimulus.3

Offset-related brain activity in the ventrolateral prefrontal cortex promotes long-term memory formation of verbal events

“…Of these, 24 (14 females; mean age ± SD: 21 ± 3 years; range: 18-29 years) took part in Experiment 1; 18 (15 females; mean age ± SD: 22 ± 3 years; range: 19-29 years) took part in Experiment 2; and 24 (17 females; mean age ± SD: 20 ± 1 year; range: 18-23 years) took part in Experiment 3. For the rTMS experiments (Experiments 1 and 3), we calculated that a minimum of 22 participants was required to detect an effect size of d = 0.74 (as in Galli et al 2017, assuming α = 0.05 and 1ß = 0.95, one-tailed paired-samples t-test), and adjusted the final sample size upwards to account for possible attrition rate. Two subjects in Experiment 1 and one subject in Experiment 3 were tested but excluded from the analyses due to low memory performance based on a-priori determined exclusion criteria (± 2 SD from the average).…”

“…All experiments followed a repeated measures design with rTMS condition as the within-subjects factor. In our previous work (Galli et al, 2017) the time of rTMS administration varied while the duration of word stimuli was set to 1000 ms in all conditions. As a consequence, it was not possible to ascertain whether rTMS effects observed immediately after word offset were driven by the offset itself, or by offset-invariant post-stimulus processes occurring around 1000 ms after the onset of the words, therefore temporally coinciding with word offset.…”

“…We conducted preliminary two-tailed pairwise comparisons to examine differences between the Vertex and the No TMS control conditions and observed no significant difference in all analyses (ps > 0.065, see Table 1 for memory performance separately for the two conditions). We therefore collapsed the two conditions to reduce the number of comparisons and achieve a unitary baseline (Galli et al, 2017).…”

“…rTMS studies demonstrated that the engagement of the lateral prefrontal cortex at different points in time during encoding, including post-stimulus time windows, is necessary for memory formation (Machizawa et al, 2010;. Importantly, one recent study showed that rTMS administered over the left ventrolateral prefrontal cortex (VLPFC) within 100 ms of the offset of word stimuli disrupted the accuracy of retrieval in a subsequent memory test (Galli et al, 2017). This effect was not evident when the stimulation was delivered during the presentation of the words or at later points in time (i.e., 200-400 ms) after their offset.…”

“…To this end, in Experiment 3 we administered VLPFC rTMS during relational encoding and hypothesized that rTMS administered at the offset of word pairs would impact subsequent associative memory. The involvement of the left VLPFC in offset-related encoding relative to online encoding was further assessed with a meta-analysis conducted on the data from both experiments of the current study and on the data reported in Galli et al (2017).…”