Transforming the Concept of Memory Reactivation
Authors: Serra E. Favila, Hongmi Lee, Brice A. Kuhl
Journal: Trends in Neurosciences (2020)

A foundational finding in the field of memory is that content-sensitive patterns of neural activity expressed during perceptual experiences are re-expressed when experiences are remembered, a phenomenon termed reactivation. However, reactivation obscures key differences in how perceptual events and memories are represented in the brain.Recent findings suggest systematic, spatial transformations of content-sensitive neural activity patterns from perception to memory retrieval. These transformations occur within sensory cortex and from sensory cortex to frontoparietal cortex.We consider why spatial transformations occur and identify critical questions to be addressed in future research. Understanding the ways in which memory representations differ from perceptual representations will critically inform theoretical accounts of memory and will help clarify how the brain recreates the past. Reactivation refers to the phenomenon wherein patterns of neural activity expressed during perceptual experience are re-expressed at a later time, a putative neural marker of memory. Reactivation of perceptual content has been observed across many cortical areas and correlates with objective and subjective expressions of memory in humans. However, because reactivation emphasizes similarities between perceptual and memory-based representations, it obscures differences in how perceptual events and memories are represented. Here, we highlight recent evidence of systematic differences in how (and where) perceptual events and memories are represented in the brain. We argue that neural representations of memories are best thought of as spatially transformed versions of perceptual representations. We consider why spatial transformations occur and identify critical questions for future research. Reactivation refers to the phenomenon wherein patterns of neural activity expressed during perceptual experience are re-expressed at a later time, a putative neural marker of memory. Reactivation of perceptual content has been observed across many cortical areas and correlates with objective and subjective expressions of memory in humans. However, because reactivation emphasizes similarities between perceptual and memory-based representations, it obscures differences in how perceptual events and memories are represented. Here, we highlight recent evidence of systematic differences in how (and where) perceptual events and memories are represented in the brain. We argue that neural representations of memories are best thought of as spatially transformed versions of perceptual representations. We consider why spatial transformations occur and identify critical questions for future research. When remembering an event from the past, it often feels as though we are re-experiencing the content of that event, bringing to mind the sensations, emotions, or thoughts that characterized the initial experience. This subjective quality of memory is paralleled by an important neural phenomenon: that content-sensitive patterns of neural activity (see Glossary) evoked during the initial experience of an event are re-expressed when that event is retrieved from memory. This phenomenon is referred to as reactivation and has been an influential tool for studying episodic memory in humans. Neural measures of reactivation have been shown to be predictive of the accuracy [1.Polyn S.M. et al.Category-specific cortical activity precedes retrieval during memory search.Science. 2005; 310: 1963-1966Crossref PubMed Scopus (416) Google Scholar, 2.Ritchey M. et al.Neural similarity between encoding and retrieval is related to memory via hippocampal interactions.Cereb. Cortex. 2013; 23: 2818-2828Crossref PubMed Google Scholar, 3.Gordon A.M. et al.Cortical reinstatement mediates the relationship between content-specific encoding activity and subsequent recollection decisions.Cereb. Cortex. 2014; 24: 3350-3364Crossref PubMed Scopus (76) Google Scholar], subjective vividness [4.St-Laurent M. et al.Distributed patterns of reactivation predict vividness of recollection.J. Cogn. Neurosci. 2015; 27: 2000-2018Crossref PubMed Scopus (30) Google Scholar,5.Kuhl B.A. Chun M.M. Successful remembering elicits event-specific activity patterns in lateral parietal cortex.J. Neurosci. 2014; 34: 8051-8060Crossref PubMed Scopus (99) Google Scholar], and consequences of memory retrieval [6.Kuhl B.A. et al.Neural reactivation reveals mechanisms for updating memory.J. Neurosci. 2012; 32: 3453-3461Crossref PubMed Scopus (0) Google Scholar, 7.Lee H. et al.Decomposing parietal memory reactivation to predict consequences of remembering.Cereb. Cortex. 2018; 29: 3305-3318Crossref Scopus (6) Google Scholar, 8.Chanales A.J.H. et al.Interference between overlapping memories is predicted by neural states during learning.Nat. Commun. 2019; 10: 5363Crossref PubMed Scopus (0) Google Scholar]. Another notable aspect of reactivation is that it can be measured in contexts such as rest [9.Tambini A. Davachi L. Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory.Proc. Natl. Acad. Sci. U. S. A. 2013; 110: 19591-19596Crossref PubMed Scopus (92) Google Scholar, 10.Schlichting M.L. Preston A.R. Memory reactivation during rest supports upcoming learning of related content.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 15845-15850Crossref PubMed Scopus (0) Google Scholar, 11.Schapiro A.C. et al.Human hippocampal replay during rest prioritizes weakly learned information and predicts memory performance.Nat. Commun. 2018; 9: 3920Crossref PubMed Scopus (27) Google Scholar] or sleep [12.Rudoy J.D. et al.Strengthening individual memories by reactivating them during sleep.Science. 2009; 326: 1079Crossref PubMed Scopus (275) Google Scholar,13.Antony J.W. et al.Cued memory reactivation during sleep influences skill learning.Nat. Neurosci. 2012; 15: 1114-1116Crossref PubMed Scopus (151) Google Scholar] when behavioral recordings are not feasible. Over the past two decades, there have been tremendous advances in both the computational sophistication and the sensitivity of the methods used to measure reactivation (Box 1), but these methods exploit the same fundamental phenomenon of a 'match' between content-sensitive neural activity patterns evoked during perception and memory retrieval. While this emphasis on the similarity between perceptual and memory-based representations is appealing and is unquestionably important, here we argue that it also provides an incomplete view of how the contents of memories are expressed in the brain during memory retrieval. In particular, because reactivation, by definition, tests for similarities between perception and retrieval, it necessarily fails to capture ways in which content representations differ between perception and memory.Box 1Methods and Approaches for Detecting ReactivationNoninvasive Neuroimaging MethodsMemory reactivation has been extensively studied using noninvasive imaging techniques [e.g., fMRI, electroencephalography (EEG), magnetoencephalography], which can simultaneously record population neural activity from large parts of the brain. Below, we detail several popular analytic approaches for measuring reactivation in neuroimaging data. All of these approaches test for similarity in profiles of neural activation during perceptual experience and memory retrieval. Notably, these methods can be applied at varying levels of specificity: stimulus category (e.g., faces vs scenes vs objects), specific exemplar (e.g., apple vs butterfly), or stimulus feature value (e.g., color: red vs yellow).Univariate ActivationBrain regions are identified for which the mean level of neural activity varies according to the stimulus content. Reactivation is demonstrated by brain regions exhibiting similar content sensitivity (changes in mean activity level) during perception and memory retrieval [19.Wheeler M.E. et al.Memory's echo: vivid remembering reactivates sensory-specific cortex.Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 11125-11129Crossref PubMed Google Scholar].Pattern SimilarityNeural activity patterns (activity across voxels or sensors) are measured during perception from a specific brain region. Patterns are then measured within the same brain region during memory retrieval. Reactivation is demonstrated by correlation between a perception pattern and a corresponding retrieval pattern exceeding the correlation between noncorresponding patterns [2.Ritchey M. et al.Neural similarity between encoding and retrieval is related to memory via hippocampal interactions.Cereb. Cortex. 2013; 23: 2818-2828Crossref PubMed Google Scholar,84.Staresina B.P. et al.Episodic reinstatement in the medial temporal lobe.J. Neurosci. 2012; 32: 18150-18156Crossref PubMed Scopus (106) Google Scholar].Decoding ModelsSupervised models are trained to learn a mapping between stimuli or stimulus classes and neural activity measured during perception. These models are then tested on neural activity measured during memory retrieval. Reactivation is demonstrated by classifier transfer from perception to retrieval (i.e., the perception-trained model accurately labeling stimuli retrieved from memory) [1.Polyn S.M. et al.Category-specific cortical activity precedes retrieval during memory search.Science. 2005; 310: 1963-1966Crossref PubMed Scopus (416) Google Scholar,22.Kuhl B.A. et al.Fidelity of neural reactivation reveals competition between memories.Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 5903-5908Crossref PubMed Scopus (0) Google Scholar].Encoding ModelsModels that specify mathematical relationships between physical stimulus properties (e.g., pixel values) and neural activity are fit to neural data measured during perception. Reactivation is demonstrated if model parameters generalize from perception to retrieval (i.e., if the perception parameters can be used to accurately predict brain activity during memory retrieval) [85.Senden M. et al.Reconstructing imagined letters from early visual cortex reveals tight topographic correspondence between visual mental imagery and perception.Brain Struct. Funct. 2019; 224: 1167-1183Crossref PubMed Scopus (11) Google Scholar]. Predicted brain activity can also be used to decode remembered stimuli (encoding–decoding) [24.Naselaris T. et al.A voxel-wise encoding model for early visual areas decodes mental images of remembered scenes.NeuroImage. 2015; 105: 215-228Crossref PubMed Scopus (101) Google Scholar,25.Bone M.B. et al.Feature-specific neural reactivation during episodic memory.Nat. Commun. 2020; 11: 1945Crossref PubMed Scopus (0) Google Scholar] or encoding models can be inverted to reconstruct remembered stimuli (inverted encoding model) [46.Ester E.F. et al.Parietal and frontal cortex encode stimulus-specific mnemonic representations during visual working memory.Neuron. 2015; 87: 893-905Abstract Full Text Full Text PDF PubMed Scopus (148) Google Scholar].Invasive Physiological and Optogenetic MethodsWhile the current article focuses on findings from noninvasive neuroimaging methods, which benefit from large-scale spatial coverage of the brain, all of the aforementioned methods can be applied to local field potential or single-cell electrophysiological activity measured invasively in humans (when treated for neurological diseases requiring electrode implants) [86.Schreiner T. Staudigl T. Electrophysiological signatures of memory reactivation in humans.Phil. Trans. R. Soc. B Biol. Sci. 2020; 37520190293Crossref PubMed Scopus (2) Google Scholar] or in animal experiments. Other approaches, such as large-scale or high-density electrophysiological recordings, are more prevalent in animal models and some approaches are restricted to animal experiments. For example, large single-unit datasets collected from rodents have been essential in characterizing the phenomenon of replay, or the temporally structured reactivation of single-cell firing sequences [62.Ólafsdóttir H.F. et al.The role of hippocampal replay in memory and planning.Curr. Biol. 2018; 28: R37-R50Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar]. Only recently has replay of single-cell firing been shown in humans [87.Vaz A.P. et al.Replay of cortical spiking sequences during human memory retrieval.Science. 2020; 367: 1131-1134Crossref PubMed Scopus (2) Google Scholar]. Optogenetic techniques, applicable in animal studies solely, have revealed that experimentally induced reactivation in rodents is sufficient to evoke memory behavior [88.Josselyn S.A. Tonegawa S. Memory engrams: recalling the past and imagining the future.Science. 2020; 367eaaw4325Crossref PubMed Scopus (39) Google Scholar]. Noninvasive Neuroimaging Methods Memory reactivation has been extensively studied using noninvasive imaging techniques [e.g., fMRI, electroencephalography (EEG), magnetoencephalography], which can simultaneously record population neural activity from large parts of the brain. Below, we detail several popular analytic approaches for measuring reactivation in neuroimaging data. All of these approaches test for similarity in profiles of neural activation during perceptual experience and memory retrieval. Notably, these methods can be applied at varying levels of specificity: stimulus category (e.g., faces vs scenes vs objects), specific exemplar (e.g., apple vs butterfly), or stimulus feature value (e.g., color: red vs yellow). Univariate Activation Brain regions are identified for which the mean level of neural activity varies according to the stimulus content. Reactivation is demonstrated by brain regions exhibiting similar content sensitivity (changes in mean activity level) during perception and memory retrieval [19.Wheeler M.E. et al.Memory's echo: vivid remembering reactivates sensory-specific cortex.Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 11125-11129Crossref PubMed Google Scholar]. Pattern Similarity Neural activity patterns (activity across voxels or sensors) are measured during perception from a specific brain region. Patterns are then measured within the same brain region during memory retrieval. Reactivation is demonstrated by correlation between a perception pattern and a corresponding retrieval pattern exceeding the correlation between noncorresponding patterns [2.Ritchey M. et al.Neural similarity between encoding and retrieval is related to memory via hippocampal interactions.Cereb. Cortex. 2013; 23: 2818-2828Crossref PubMed Google Scholar,84.Staresina B.P. et al.Episodic reinstatement in the medial temporal lobe.J. Neurosci. 2012; 32: 18150-18156Crossref PubMed Scopus (106) Google Scholar]. Decoding Models Supervised models are trained to learn a mapping between stimuli or stimulus classes and neural activity measured during perception. These models are then tested on neural activity measured during memory retrieval. Reactivation is demonstrated by classifier transfer from perception to retrieval (i.e., the perception-trained model accurately labeling stimuli retrieved from memory) [1.Polyn S.M. et al.Category-specific cortical activity precedes retrieval during memory search.Science. 2005; 310: 1963-1966Crossref PubMed Scopus (416) Google Scholar,22.Kuhl B.A. et al.Fidelity of neural reactivation reveals competition between memories.Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 5903-5908Crossref PubMed Scopus (0) Google Scholar]. Encoding Models Models that specify mathematical relationships between physical stimulus properties (e.g., pixel values) and neural activity are fit to neural data measured during perception. Reactivation is demonstrated if model parameters generalize from perception to retrieval (i.e., if the perception parameters can be used to accurately predict brain activity during memory retrieval) [85.Senden M. et al.Reconstructing imagined letters from early visual cortex reveals tight topographic correspondence between visual mental imagery and perception.Brain Struct. Funct. 2019; 224: 1167-1183Crossref PubMed Scopus (11) Google Scholar]. Predicted brain activity can also be used to decode remembered stimuli (encoding–decoding) [24.Naselaris T. et al.A voxel-wise encoding model for early visual areas decodes mental images of remembered scenes.NeuroImage. 2015; 105: 215-228Crossref PubMed Scopus (101) Google Scholar,25.Bone M.B. et al.Feature-specific neural reactivation during episodic memory.Nat. Commun. 2020; 11: 1945Crossref PubMed Scopus (0) Google Scholar] or encoding models can be inverted to reconstruct remembered stimuli (inverted encoding model) [46.Ester E.F. et al.Parietal and frontal cortex encode stimulus-specific mnemonic representations during visual working memory.Neuron. 2015; 87: 893-905Abstract Full Text Full Text PDF PubMed Scopus (148) Google Scholar]. Invasive Physiological and Optogenetic Methods While the current article focuses on findings from noninvasive neuroimaging methods, which benefit from large-scale spatial coverage of the brain, all of the aforementioned methods can be applied to local field potential or single-cell electrophysiological activity measured invasively in humans (when treated for neurological diseases requiring electrode implants) [86.Schreiner T. Staudigl T. Electrophysiological signatures of memory reactivation in humans.Phil. Trans. R. Soc. B Biol. Sci. 2020; 37520190293Crossref PubMed Scopus (2) Google Scholar] or in animal experiments. Other approaches, such as large-scale or high-density electrophysiological recordings, are more prevalent in animal models and some approaches are restricted to animal experiments. For example, large single-unit datasets collected from rodents have been essential in characterizing the phenomenon of replay, or the temporally structured reactivation of single-cell firing sequences [62.Ólafsdóttir H.F. et al.The role of hippocampal replay in memory and planning.Curr. Biol. 2018; 28: R37-R50Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar]. Only recently has replay of single-cell firing been shown in humans [87.Vaz A.P. et al.Replay of cortical spiking sequences during human memory retrieval.Science. 2020; 367: 1131-1134Crossref PubMed Scopus (2) Google Scholar]. Optogenetic techniques, applicable in animal studies solely, have revealed that experimentally induced reactivation in rodents is sufficient to evoke memory behavior [88.Josselyn S.A. Tonegawa S. Memory engrams: recalling the past and imagining the future.Science. 2020; 367eaaw4325Crossref PubMed Scopus (39) Google Scholar]. One obvious way in which memory-based and perceptual representations might differ is in terms of the amount of information they contain, with memory-based representations presumably being a weaker or degraded version of perceptual representations. Empirically, this might manifest, for example, as a reduced ability to decode the content of an event from neural activity patterns evoked during retrieval compared with patterns evoked during perception. However, a number of recent studies have demonstrated clear violations of this idea: specifically, some brain regions contain more information about the content of an experience when that experience is being retrieved from memory compared with when it is perceptually experienced [14.Steel A. et al.An interface between spatial memory and scene perception in posterior cerebral cortex.bioRxiv. 2020; (Published online May 26, 2020. https://doi.org/10.1101/2020.05.25.115147)PubMed Google Scholar, 15.Long N.M. et al.Hippocampal mismatch signals are modulated by the strength of neural predictions and their similarity to outcomes.J. Neurosci. 2016; 36: 12677-12687Crossref PubMed Scopus (22) Google Scholar, 16.Xiao X. et al.Transformed neural pattern reinstatement during episodic memory retrieval.J. Neurosci. 2017; 37: 2986-2998Crossref PubMed Scopus (24) Google Scholar, 17.Favila S.E. et al.Parietal representations of stimulus features are amplified during memory retrieval and flexibly aligned with top-down goals.J. Neurosci. 2018; 38: 7809-7821Crossref PubMed Scopus (3) Google Scholar]. The clear implication of this is that measures of reactivation, which only test whether activity patterns evoked during retrieval are similar to those evoked during perception, will systematically underestimate the amount, strength, or qualities of content representations during retrieval. In this opinion article, we argue that there is emerging evidence that content representations during memory retrieval are spatially transformed versions of content representations originally expressed during perception. We use this idea of spatial transformation to emphasize that content information: (i) is expressed in different brain regions during perception and memory retrieval and, (ii) that these differences in spatial localization are systematic (or predictable) as opposed to random noise or signal degradation during memory retrieval (Figure 1). While the possibility of systematic differences in content representations during perception and memory retrieval has, to date, been overshadowed by the more dominant idea of reactivation, it is important to note that cognitive theories of episodic memory have long argued that memory retrieval is more of a constructive act than a reproductive act [18.Schacter D.L. et al.The cognitive neuroscience of constructive memory.Annu. Rev. Psychol. 1998; 49: 289-318Crossref PubMed Google Scholar]. Thus, there is a strong theoretical motivation for moving beyond measurements that only index the degree to which content representations at retrieval resemble those at perception and moving toward approaches that characterize how and why content representations at retrieval differ from those at perception. In subsequent sections of this article, we describe some of the recent evidence supporting the specific proposal of spatial transformation from perception to memory. We consider several accounts of why spatial transformations occur and highlight several avenues for future research. We argue that characterizing and understanding perception-to-memory transformations (spatial and otherwise) represents a logical, timely, and important next step for the field. While memory reactivation has been reported in many parts of the human brain, it has been most frequently measured in sensory areas and visual cortex in particular. Early studies demonstrated that visual cortex is active both during visual perception and during retrieval of visual memories [19.Wheeler M.E. et al.Memory's echo: vivid remembering reactivates sensory-specific cortex.Proc. Natl. Acad. Sci. U. S. A. 2000; 97: 11125-11129Crossref PubMed Google Scholar], demonstrating a coarse-level reactivation of the sensory modality of experience (e.g., vision versus audition). More recently, studies have established reactivation of increasingly fine-grained information within visual cortical areas. For example, numerous studies have shown that patterns of activity in ventral temporal cortex that reflect the visual category of a stimulus (e.g., face versus scene versus object) are reactivated during retrieval of that stimulus [1.Polyn S.M. et al.Category-specific cortical activity precedes retrieval during memory search.Science. 2005; 310: 1963-1966Crossref PubMed Scopus (416) Google Scholar,20.Ranganath C. et al.Inferior temporal, prefrontal, and hippocampal contributions to visual working memory maintenance and associative memory retrieval.J. Neurosci. 2004; 24: 3917-3925Crossref PubMed Scopus (251) Google Scholar, 21.O'Craven K.M. Kanwisher N. Mental imagery of faces and places activates corresponding stimulus-specific brain regions.J. Cogn. Neurosci. 2000; 12: 1013-1023Crossref PubMed Scopus (638) Google Scholar, 22.Kuhl B.A. et al.Fidelity of neural reactivation reveals competition between memories.Proc. Natl. Acad. Sci. U. S. A. 2011; 108: 5903-5908Crossref PubMed Scopus (0) Google Scholar]. Further, patterns of neural activity in early visual areas (e.g., V1) that reflect low-level stimulus properties such as spatial location, spatial frequency, edges, and orientation, are also reactivated during retrieval [23.Kosslyn S.M. et al.Topographical representations of mental images in primary visual cortex.Nature. 1995; 378: 496-498Crossref PubMed Google Scholar, 24.Naselaris T. et al.A voxel-wise encoding model for early visual areas decodes mental images of remembered scenes.NeuroImage. 2015; 105: 215-228Crossref PubMed Scopus (101) Google Scholar, 25.Bone M.B. et al.Feature-specific neural reactivation during episodic memory.Nat. Commun. 2020; 11: 1945Crossref PubMed Scopus (0) Google Scholar, 26.Bosch S.E. et al.Reinstatement of associative memories in early visual cortex is signaled by the hippocampus.J. Neurosci. 2014; 34: 7493-7500Crossref PubMed Scopus (62) Google Scholar]. The common thread among these examples of visual cortical reactivation is that the same content-sensitive patterns of activity evoked during perception are re-expressed during memory retrieval. Yet, results from a number of recent studies suggest that there are subtle, but systematic differences in the spatial localization of content information within visual cortex during perception and memory retrieval. In particular, several studies have found that scene-selective responses during perception are located posterior to scene-selective responses during memory retrieval. For example, a meta-analysis of over 100 functional magnetic resonance imaging (fMRI) studies found that scene perception recruits relatively posterior aspects of the parahippocampal place area (PPA), whereas retrieving scenes from memory recruits relatively anterior aspects of PPA [27.Baldassano C. et al.Two distinct scene-processing networks connecting vision and memory.eNeuro. 2016; 3 (ENEURO.0178-16.2016)Crossref PubMed Scopus (39) Google Scholar]. In an unpublished study, this striking dissociation was replicated in a paradigm that directly compared perception and memory retrieval using a within-subjects design [14.Steel A. et al.An interface between spatial memory and scene perception in posterior cerebral cortex.bioRxiv. 2020; (Published online May 26, 2020. https://doi.org/10.1101/2020.05.25.115147)PubMed Google Scholar]. Similar posterior (perception) to anterior (memory retrieval) shifts have been observed in other scene-selective areas, including lateral occipital and medial parietal areas [14.Steel A. et al.An interface between spatial memory and scene perception in posterior cerebral cortex.bioRxiv. 2020; (Published online May 26, 2020. https://doi.org/10.1101/2020.05.25.115147)PubMed Google Scholar,28.Silson E.H. et al.A posterior–anterior distinction between scene perception and scene construction in human medial parietal cortex.J. Neurosci. 2019; 39: 705-717Crossref PubMed Scopus (0) Google Scholar]. Resting state fMRI analyses have shown that anterior and posterior aspects of ventral, lateral, and medial scene-selective areas have different connectivity profiles with the rest of the brain, consistent with the idea that scene perception and scene memory are supported by segregated visual cortical networks [14.Steel A. et al.An interface between spatial memory and scene perception in posterior cerebral cortex.bioRxiv. 2020; (Published online May 26, 2020. https://doi.org/10.1101/2020.05.25.115147)PubMed Google Scholar,27.Baldassano C. et al.Two distinct scene-processing networks connecting vision and memory.eNeuro. 2016; 3 (ENEURO.0178-16.2016)Crossref PubMed Scopus (39) Google Scholar, 28.Silson E.H. et al.A posterior–anterior distinction between scene perception and scene construction in human medial parietal cortex.J. Neurosci. 2019; 39: 705-717Crossref PubMed Scopus (0) Google Scholar, 29.Baldassano C. et al.Differential connectivity within the parahippocampal place area.NeuroImage. 2013; 75: 228-237Crossref PubMed Scopus (84) Google Scholar]. Related work has suggested that this posterior-to-anterior division between visual perception and visual memory extends to stimulus classes other than scenes, such as objects, and to aspects of lateral and ventral temporal cortex outside of the scene network [30.Lee S.H. et al.Disentangling visual imagery and perception of real-world objects.NeuroImage. 2012; 59: 4064-4073Crossref PubMed Scopus (89) Google Scholar,31.Bainbridge W.A. et al.Distinct representational structure and localization for visual encoding and recall during visual imagery.bioRxiv. 2020; (Published online April 21, 2020. https://doi.org/10.1101/842120)Google Scholar]. Collectively, these studies reveal a shift in the spatial localization of content-sensitive responses during perception and memory retrieval in the visual system. Specifically, information about a stimulus is preferentially expressed in different regions of visual cortex, depending on whether that stimulus is currently available to sensory receptors or recalled from long-term memory. Importantly, the fact that some regions of the visual system contain more information about remembered stimuli than they do about perceived stimuli is fundamentally inconsistent with the idea of reactivation. Moreover, these differences in spatial localization are highly systematic (as opposed to random noise or signal degradation) and generalize across different classes of stimuli and visual regions. As such, these findings strongly suggest that content representations during perception are re-expressed in a spatially transformed manner during memory retrieval. Though memory reactivation has been most consistently observed in sensory areas, recent applications of pattern-based analysis methods have revealed robust, content-sensitive reactivation in frontoparietal regions [5.Kuhl B.A. Chun M.M. Successful remembering elicits event-specific activity patterns in lateral parietal cortex.J. Neurosci. 2014; 34: 8051-8060Crossref PubMed Scopus (99) Google Scholar,7.Lee H. et al.Decomposing parietal memory reactivation to predict consequences of remembering.Cereb. Cortex. 2018; 29: 3305-3