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Long-Term Memory Prepares Neural Activity for Perception

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Long-Term Memory Prepares Neural Activity for Perception Long-term memory prepares neural activity for perception Mark G. Stokes1, Kathryn Atherton, Eva Zita Patai, and Anna Christina Nobre Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom AUTHOR SUMMARY Our memories shape how we see We test these hypotheses by the world. As we learn the reg- using an experimental task in ularities in our environment, we which experience can be used to build expectations that help us guide preparatory shifts to opti- process new information. These mize perception. This protocol expectations, which become allows us to isolate memory- coded in our long-term memory guided attentional preparation. (LTM), provide a rich source of First, participants performed predictive information for opti- a search task in which they mizing perception for goal-di- learned the location of a specific rected behavior; however, target stimulus within a large studies have not yet identified set (80 or more) of naturalistic Fig. P1. Memories that predict task-relevant locations trigger the neural mechanisms that in- mechanisms of spatial attention. (A) In separate EEG and fMRI visual scenes. On a separate day, tegrate learned predictions with experiments, participants performed a memory-guided attention task participants performed a mem- attentional control. Here, we in which previously learned scenes were used to cue attention to the ory-guided orienting task (Fig. demonstrate that the contents of remembered target location. (B) Detection sensitivity (bars) of P1A) while we acquired elec- LTM may optimize perception a subsequent target was significantly enhanced by spatially predictive troencephalogram (EEG) (n = by modulating anticipatory brain memories, as were response latencies (▼). (C) Following the memory 16), which records the electrical states. By using a paradigm that cue, and in preparation for the memory-predicted target, neural activity of the brain, or function integrates LTM and attentional activity was enhanced in brain areas that represent the remembered magnetic resonance imaging fi target location. (D) Finally, activity in parietal and frontal areas was (fMRI; n = 20), which measures orienting, we rst show that the also associated with memory-guided control over attention. contents of LTM sharpen per- increases in blood flow relating ceptual sensitivity for targets to brain activity. Whereas stan- presented at remembered spatial locations. Next, we use imaging dard covert-orienting tasks use explicit spatial cues to direct at- methods with complementary temporal and spatial resolution, to tention, in the memory-guided orienting task, the learned scenes show how memory triggers preparatory neural states in the visual provided a rich context for directing spatial attention in prepa- cortex. Our research shows that the high-level frontoparietal ration for target detection. Scenes that contained a search tar- control network is important in guiding attentional biases get during the learning task constituted a valid memory cue that according to memory and suggests that the hippocampus could predicted the target location for the detection task. In contrast, provide a crucial link between past and future goals in memory- scenes that did not contain a target during learning constituted guided attention. a neutral memory cue that did not provide any predictive in- Previous investigations into the neural mechanisms that opti- formation about the likely location of the subsequent target mize perception on the basis of task goals have typically used stimulus. Immediately after completing the orienting task, par- explicit cues to manipulate attention, such as an arrow pointing to ticipants performed an explicit memory test, allowing us to the likely location of a subsequent target stimulus. However, in identify which scenes were associated with accurate recollection everyday life, we rarely enjoy the benefit of such explicit cues and of the target locations. must rely on our own experiences, which are stored in LTM. Behavioral analyses confirmed that participants were able to The biological relevance of experience-based perceptual bi- learn the spatial locations of targets embedded in these complex asing has long been recognized by theoretical accounts (1). scenes. Participants found more target stimuli as they progressed However, few studies have directly examined the neural mech- in the learning task, with a corresponding decrease in search anisms that integrate memory and attentional control. Studies on times. This learning profile, which was observed for the EEG and contextual cueing highlight the important relationship between fMRI experiments, demonstrates that participants could use past experience and perception (2). When participants search their memories of the target location to reduce the search for a target among distractor stimuli, search times decrease for demands. Moreover, the results of the memory test, performed stimulus configurations that have been repeatedly used in an after the orienting task, further confirmed the robust acquisition experiment. Moreover, the benefit of contextual cueing depends on memory-related brain areas, including the hippocampus. Building on previous evidence from our own laboratory (3), we Author contributions: M.G.S. and A.C.N. designed research; M.G.S., K.A., E.Z.P., and A.C.N. suggest that LTM for a specific behaviorally relevant spatial lo- performed research; M.G.S. and A.C.N. analyzed data; and M.G.S. and A.C.N. wrote the paper. cation within a particular context triggers a shift in spatial at- fl tention that modulates the baseline activity in the perceptual The authors declare no con ict of interest. cortex to prioritize processing at the remembered target location. This Direct Submission article had a prearranged editor. Furthermore, we hypothesize that memory-related shifts in Freely available online through the PNAS open access option. spatial attention are triggered via a top-down control circuit that 1To whom correspondence should be addressed. E-mail: [email protected]. includes the frontoparietal and limbic brain areas, such as the See full research article on page E360 of www.pnas.org. hippocampus, that support LTM. Cite this Author Summary as: PNAS 10.1073/pnas.1108555108. 1838–1839 | PNAS | February 7, 2012 | vol. 109 | no. 6 www.pnas.org/cgi/doi/10.1073/pnas.1108555108 Downloaded by guest on October 2, 2021 and retention of LTM for target locations. Having thus dem- shift in the focus of attention. We next investigated how memory PNAS PLUS onstrated that participants were able to learn behaviorally rele- can control this shift in spatial attention. vant spatial locations in a large set of naturalistic scenes, we then A network of frontal and parietal brain areas previously im- show that these memories are used to prioritize perceptual plicated in the control of visual spatial attention is a good can- processing at memory-predicted locations. didate for mediating between the spatial memory signal and the To measure the influence of memory-guided attention on control of preparatory activity in visual cortex. In the current perception, we compared perceptual sensitivity for detecting experiment, we successfully dissociated activity relating to cue targets in the orienting task presented after valid memory cues, and target events, allowing us to confirm that valid memory cues or following neutral memory cues. Positive cueing effects were activate parietal and frontal areas more than neutral memory evident in the EEG (Fig. P1B) and fMRI experiments. These cues do (Fig. P1D). Hence, signals from the frontoparietal cortex reliable changes in perceptual sensitivity show that memory- could provide top-down modulation of the visual cortex, result- guided preparatory attention directly influences perceptual ing in preparatory biases that would optimize target processing. sensitivity. This brings us to the main question: how do pre- The use of experience to guide future behavior is probably dictions, stored in LTM, fine-tune perceptual sensitivity? To one of the most general optimizing principles in neuroscience answer this, we imaged the neural dynamics and activation pat- (1, 5), critically underlying adaptive intelligent behavior. Here, terns triggered by memory cues during the orienting task. we address the important link between predictions derived We first used EEG to detect anticipatory biases in neural ac- from experience and another fundamental optimizing principle, tivity when a participant remembered the target location. Pre- attentional control. In two complementary experiments, we paratory changes were characterized by a shift in low-frequency demonstrated how experiences shape perceptions via shifts in neural oscillations (∼10 Hz) in visual brain areas that represent baseline visual activity, to optimize the sensory analysis of task- the remembered spatial location (Fig. P1C). Previous research relevant information. The process of turning memories into demonstrates that dynamics within this “alpha” frequency range perceptual biases involves an integrated network of frontopar- provide a plausible neurophysiological mechanism for fine-tun- ietal and limbic brain areas. The top-down biasing of perceptual ing the sensitivity of the visual cortex to bias information pro- cortices via the integration of memory signals into a multisen- cessing at spatial locations that are most likely to be behaviorally sory network involved in the control of spatial attention relevant (4). The results of this experiment provide important
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