Early top-down control of internal selection induced by retrospective cues in visual working memory: advantage of peripheral over central cues

Abstract

Attention can be deployed among external sensory stimuli or internal working memory (WM) representations, and recent primate studies have revealed that these external and internal selections share a common neural basis in the prefrontal cortex (PFC). However, it remains to be elucidated how PFC implements these selections, especially in humans. The present study aimed to further investigate whether PFC responded differentially to the peripheral and central retrospective cues (retro-cues) that induced attention selection among WM representations. To achieve this, we combined magnetoencephalography (MEG, Experiment 1) and transcranial magnetic stimulation (TMS, Experiment 2) with an orientation-recall paradigm. Experiment 1 found that a peripheral retro-cue with 100% reliability had a greater benefit on WM performance than a central retro-cue, while this advantage of peripheral over central cues vanished when the cue reliability dropped to 50% (non-informative). MEG source analysis indicated that the 100% peripheral retro-cue elicited earlier (∼125 ms) PFC responses than the central retro-cue (∼275 ms). Meanwhile, Granger causality analysis showed that PFC had earlier (0–200 ms) top-down signals projecting to the superior parietal lobule (SPL) and the lateral occipital cortex (LOC) after the onset of peripheral retro-cues, while these top-down signals appeared later (300–500 ms) after the onset of central retro-cues. Importantly, PFC activity within this period of 300–500 ms correlated with the peripheral advantage in behavior. Moreover, Experiment 2 applied TMS at different time points to test the causal influence of brain activity on behavior and found that stimulating PFC at 100 ms abolished the behavioral benefit of the peripheral retro-cue, as well as its advantage over the central retro-cue. Taken together, our results suggested that the advantage of peripheral over central retro-cues in the mnemonic domain is realized through faster top-down control from PFC, which challenged traditional opinions that the top-down control of attention on WM required at least 300 ms to appear. The present study highlighted that in addition to the causal role of PFC in attention selection of WM representations, timing was critical as well and faster was better.