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

Abstract

Recent evidence suggests that brain activity following the offset of a stimulus during encoding contributes to long-term memory formation, however the exact mechanisms underlying offset-related encoding are still unclear. Here we used repetitive transcranial magnetic stimulation (rTMS) to investigate offset-related activity in the left ventrolateral prefrontal cortex (VLPFC). rTMS was administered at different points in time around stimulus offset while male and female participants encoded visually-presented words (first rTMS experiment) or pairs of words (second rTMS experiment) and the analyses focused on the effects of the stimulation on subsequent memory performance. The results show that rTMS administered at the offset of the stimuli, but not during online encoding, disrupted subsequent memory performance. In the first experiment we show that rTMS specifically disrupted encoding mechanisms initiated by the offset of the stimuli rather than general, post-stimulus processes. In the second experiment, we show a robust decline in associative memory performance when rTMS was delivered at the offset of the word pairs, suggesting that offset-related encoding may contribute to the binding of information into an episodic memory trace. A meta-analysis conducted on the two studies and on a previously published dataset confirmed that the involvement of the left VLPFC in memory formation is initiated by the offset of the stimulus. The offset of the stimulus may represent an event boundary that promotes the reinstatement of the previously experienced event and episodic binding.\n\nSIGNIFICANCE STATEMENTHow well an event is encoded predicts how well it is remembered, and verbal encoding is an important part of everyday memory that, if disrupted, can lead to difficulties and disorders. The timing of encoding processes relative to the presentation of an event is important for successful retrieval, and little is known about the interval immediately after an events presentation (post-stimulus offset) which is thought to involve critical encoding processes in the VLPFC and hippocampus. The current studies demonstrate that indeed, verbal encoding processes in the VLPFC that are necessary for memory formation are triggered by the offset of the word, and these processes may involve VLPFC-hippocampal interactions that promote binding of event features into a single, coherent memory trace.