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. O ur expectations shape how we see the world. From the earliest pioneers in perception (e.g., ref. 1), it has long been appreciated that past experience guides perceptual processing and decision-making. Indeed, the statistical regularities of the environment, extracted over past experience and coded in longterm memory (LTM), provide a rich source of predictive information that could be exploited to optimize perception for goal-directed behavior (2-4).Studies of selective attention provide an important framework for understanding the dynamic changes in neural processing that optimize perceptual analysis for goal-specific input. In particular, influential theories suggest that modulations in baseline neural activity in sensory cortex bias perceptual processing in favor of behaviorally relevant information (5-7). For example, a cue stimulus that provides information about the likely location of a target triggers a shift in baseline activity for neurons that represent the cued position (8-11), thereby increasing the neural sensitivity for subsequent stimulation at the attended region of space (10, 11). However, in everyday life, we rarely enjoy the benefit of explicit cues to guide our attention. More typically, we must rely on our own past experiences, stored in LTM, to build the predictions that shape perception for goal-directed behavior.Despite the obvious biological relevance of experience-based perceptual biasing, few studies have directly examined how memory influences attentional control. Studies of contextual cueing (2) demonstrate a close relationship between past experience and visual search efficiency: search times decrease with repeated exposure to the same stimulus configurations, even when repetitions are not explicitly processed (12). Contextual cueing effects are particularly compelling for detail-rich naturalistic scen...

Enhancing long-term memory with stimulation tunes visual attention in one trial

“…The prevailing theoretical view is that working memory representations of target objects provide topdown control of attention as we perform visual search for these objects embedded in arrays of distractors (3)(4)(5)(6)(7). However, an alternative view is that long-term memory representations play a critical role in the top-down control of attention, enabling us to guide attention based on the more enduring representations of this memory store (8)(9)(10)(11)(12)(13)(14)(15)(16). To distinguish between these competing theoretical perspectives, we used transcranial direct-current stimulation (tDCS) to manipulate activity in the brain causally (17), and combined this causal manipulation of neural activity with electrophysiological measurements that are hypothesized to index the working memory and long-term memory representations that guide visual attention to task-relevant target objects.…”

The Neural Mechanisms of Prediction in Visual Search

“…Early research in visual search focused mostly on examining how bottom-up stimulus properties determined visual search efficiency (Treisman and Gelade 1980). However, visual search efficiency is also strongly shaped by our prior knowledge of the scene, either derived from scene context (Biederman 1972;Bar 2004) or from past experience with a scene (Chun and Jiang 1998;Stokes et al 2012). Both of these factors provide a rich source of predictive information about the visual world that can be used to guide and optimize visual selection (Summerfield and de Lange 2014).…”

“…First, what is the nature of the prediction? Do initial glimpses give rise to a spatial prediction ("This location may contain a target"), thus prioritizing a particular part of visual space for subsequent processing (Chun and Jiang 1998;Stokes et al 2012)? Such a prioritization would likely be reflected in a hemispheric lateralization of posterior alpha-band (8-12 Hz) activity (Worden et al 2000;Thut et al 2006).…”

How ageing changes the mnemonic bias of visual behaviour

“…Neural mechanisms of feature-based memory-based biases of visual selection are dissociable from the dorsal and ventral fronto-parietal networks involved in stimulus-driven attentional control (Corbetta and Shulman, 2002). Feature-based mnemonic biasing also involve frontal substrates but, crucially, subcortical substrates in thalamic nuclei can play a fundamental role (de Bourbon-Teles et al, 2016;, including anterior and ventrolateral thalamus involved in memory and oculomotor control (Aggleton et al, 2010;Kunimatsu and Tanaka, 2010), and also the hippocampus (Soto et al 2012;Stokes et al, 2012). Previous studies of attention control in ageing have mainly focused on deficient deficient frontoparietal control networks involved in attention and the compensatory mechanisms in these frontoparietal networks that may be !…”