Long-term memory prepares neural activity for perception

Abstract

Past experience provides a rich source of predictive information about the world that could be used to guide and optimize ongoing perception. However, the neural mechanisms that integrate information coded in long-term memory (LTM) with ongoing perceptual processing remain unknown. Here, we explore how the contents of LTM optimize perception by modulating anticipatory brain states. By using a paradigm that integrates LTM and attentional orienting, we first demonstrate that the contents of LTM sharpen perceptual sensitivity for targets presented at memory-predicted spatial locations. Next, we examine oscillations in EEG to show that memory-guided attention is associated with spatially specific desynchronization of alpha-band activity over visual cortex. Additionally, we use functional MRI to confirm that target-predictive spatial information stored in LTM triggers spatiotopic modulation of preparatory activity in extrastriate visual cortex. Finally, functional MRI results also implicate an integrated cortical network, including the hippocampus and a dorsal frontoparietal circuit, as a likely candidate for organizing preparatory states in visual cortex according to the contents of LTM.

Fig. 1.

Experimental protocol for memory-guided attention. (A) In both EEG and fMRI experiments, participants first completed a learning task in which they searched for a target stimulus that was embedded within naturalistic scenes. Targets were presented on the right (Right Memory), left (Left Memory) or not at all (Neutral Memory). (B) Over repeated sessions, participants found, and learned, the location of target stimuli. The learning profile from the EEG experiment is plotted for search accuracy (left y axis, red) and search time (right y axis, blue) as a function of training session number (x axis). (C) On the following day, participants performed an attention task in which scenes from the initial learning task were used to cue the location of a subsequent target. The first scene was always presented without the target stimulus, whereas the second scene contained a target on 50% of trials. On target-present trials, previously learned locations were 100% predictive of the subsequent target location. Consequently, valid memory cue scenes could be used to predict the precise location of the subsequent target, whereas memories for neutral cues contained no task-relevant spatial information. (D) Behavioral data are shown for the EEG experiment, with sensitivity (left y axis, bars) and RT (right y axis, triangles) plotted as a function memory condition (memory vs. neutral). Detection sensitivity was higher for spatially predictive memories, and RTs were shorter. Error bars represent ±1 SEM.

Fig. 2.

Memory predictions trigger contralateral alpha-desynchronization in posterior electrodes. (A) EEG recordings demonstrate that memory cues trigger spatially specific desynchronization of alpha-band oscillations in posterior electrodes, including PO7/PO8. The scalp topography of cue-specific differences (left − right cue; 650–750 ms) in alpha power is shown projected across a 3D scalp surface. (B) Time-course analysis of alpha power in lateralized posterior electrodes, PO7 (in red) and PO8 (in blue), illustrates how contralateral desynchronization emerges at approximately 400 ms after the cue onset. Positive values reflect contralateral desynchronization in the left hemisphere, whereas negative values reflect desynchronization in the right hemisphere, and shading represents ±1 SEM.

Fig. 3.

Memory predictions increase BOLD-related activity in contralateral visual areas. (A) Behavioral analysis of fMRI experiment confirmed that detection sensitivity was enhanced for targets presented at memory-predicted locations, relative to memory-neutral locations. Detection sensitivity (left y axis, bars) and RT (right y axis, triangles) are plotted as a function memory condition (memory valid vs. neutral). (B) Analysis of the BOLD response revealed evidence of spatially specific biases in preparatory visual activity: memory cues elicited increased activity in contralateral subregions of visual cortex, particularly in extrastriate visual areas. Data contrasting left vs. right views are shown on the occipital surface, extracted and flattened using Freesurfer (Materials and Methods) (C) Spatially specific cue-related activity is shown for specific visual areas (text provides details). Error bars represent ±1 SEM.

Fig. 4.

Control network for memory-guided attention. (A) Whole-brain analyses revealed a network of parietal and frontal brain areas that are more active in response to valid memory cues, relative to memory-neutral cues (valid > neutral, P_FDR < 0.05). (B) More specific ROI analyses focused on activation profiles within key nodes of an attentional network, IPS and FEF, that were previously associated with memory-guided orienting (16). Beta parameter estimates are plotted as a function of memory condition (valid vs. neutral) and event type (cue vs. target). Validity effects were specific to the cue event in both ROIs. (C) Data were also analyzed for the hippocampus, defined according to the coordinates from Summerfield et al. (16), which are also shown as a function of memory condition (valid vs. neutral) and event type (cue vs. target). Hippocampal activity was specific to cue events, and there was a trend for a validity effect for cues but not targets. Error bars represent ±1 SEM.

Fig. P1.

Memories that predict task-relevant locations trigger mechanisms of spatial attention. (A) In separate EEG and fMRI experiments, participants performed a memory-guided attention task in which previously learned scenes were used to cue attention to the remembered target location. (B) Detection sensitivity (bars) of a subsequent target was significantly enhanced by spatially predictive memories, as were response latencies (▼). (C) Following the memory cue, and in preparation for the memory-predicted target, neural activity was enhanced in brain areas that represent the remembered target location. (D) Finally, activity in parietal and frontal areas was also associated with memory-guided control over attention.