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Distributed Representations in Memory: Insights from Functional Brain Imaging
Open accessAbstract
Forging new memories for facts and events, holding critical details in mind on a moment-to-moment basis, and retrieving knowledge in the service of current goals all depend on a complex interplay between neural ensembles throughout the brain. Over the past decade, researchers have increasingly utilized powerful analytical tools (e.g., multivoxel pattern analysis) to decode the information represented within distributed functional magnetic resonance imaging activity patterns. In this review, we discuss how these methods can sensitively index neural representations of perceptual and semantic content and how leverage on the engagement of distributed representations provides unique insights into distinct aspects of memory-guided behavior. We emphasize that, in addition to characterizing the contents of memories, analyses of distributed patterns shed light on the processes that influence how information is encoded, maintained, or retrieved, and thus inform memory theory. We conclude by highlighting open questions about memory that can be addressed through distributed pattern analyses.
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“So-called subsequent memory paradigms [141] have yielded several markers that predicted the later voluntary recollection of information [142], or the involuntary retrieval of experimental trauma [143–145].”
From Multiple memory systems, multiple time points: How science can inform treatment to control the expression of unwanted emotional memories (2018) · cites this paper as [142]
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Self-citationModerate levels of activation lead to forgetting in the think/no-think paradigm
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Self-citationCortical Mechanisms of Cognitive Control for Shifting Attention in Vision and Working Memory
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“…and memory, these methods have revolutionized researchers’ abilities to ask questions about how information is encoded, maintained, and retrieved at various stages of processing in ways that test and inform psychological theories of memory and perception (Kay et al. 2008; Rissman and Wagner 2012).”
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Similar patterns of neural activity predict memory function during encoding and retrieval
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Self-citationIs Color Experience Cognitively Penetrable?
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BackgroundMemory guides the processing of event changes for older and younger adults.
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Model-based whole-brain effective connectivity to study distributed cognition in health and disease
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BackgroundAge Differences In Retrieval-Related Reinstatement Reflect Age-Related Dedifferentiation At Encoding
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BackgroundDecomposing Parietal Memory Reactivation to Predict Consequences of Remembering
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Reggente, N., Essoe, J. K.-Y., Baek, Y. H., & Rissman, J. (2019) · Journal of Cognitive Enhancement · doi:10.1007/s41465-019-00141-8 · Cited by 63
Self-citationExploring the neurocognitive basis of episodic recollection in autism
Cooper, R. A., & Simons, J. S. (2018) · Psychonomic Bulletin & Review · doi:10.3758/s13423-018-1504-z · Cited by 56
Human Verbal Memory Encoding Is Hierarchically Distributed in a Continuous Processing Stream
Kucewicz, M. T., Saboo, K., Berry, B. M., Křemen, V., Miller, L. R., Khadjevand, F., Inman, C. S., Wanda, P. A., Sperling, M. R., Gorniak, R., et al. (2019) · eNeuro · doi:10.1523/eneuro.0214-18.2018 · Cited by 51
“These multi-modal computations are distributed across multiple cortical areas (Mesulam, 1990; Gaffan, 2002; Rissman and Wagner, 2012) and stored as induced changes in neural activity.”
BackgroundJiang, X., Shamie, I., Doyle, W., Friedman, D. J., Dugan, P. C., Devinsky, O., Eskandar, E. N., Cash, S. S., Thesen, T., & Halgren, E. (2017) · Scientific Reports · doi:10.1038/s41598-017-17469-w · Cited by 61
More is less: increased processing of unwanted memories facilitates forgetting
Wang, T. H., Placek, K., & Lewis‐Peacock, J. A. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2033-18.2019 · Cited by 51
“In our experiment, we hypothesized that deliberate forgetting is facilitated by the weakening of moderately active memories represented in the sensory cortex, specifically in the ventral temporal cortex (VTC; Rissman and Wagner, 2012; D’Esposito and Postle, 2015; Christophel et al., 2017).”
BackgroundMethodLong, N. M., & Kahana, M. J. (2016) · Journal of Experimental Psychology Learning Memory and Cognition · doi:10.1037/xlm0000300 · Cited by 52
Memory Retrieval in Mice and MenPreprint
Ben-Yakov, A., Dudai, Y., & Mayford, M. R. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021790 · Cited by 54
Koen, J. D., & Rugg, M. D. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4099-15.2016 · Cited by 55
Pallarés, V., Insabato, A., Sanjuán, A., Kühn, S., Mantini, D., Deco, G., & Gilson, M. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.04.070 · Cited by 42
“We quantified the clustering degree of these clouds using a silhouette coefficient for each session, ranging from 1 for poor clustering to 1 for perfect clustering (Rousseeuw, 1987); see Section 4.3.3 in Methods.”
BackgroundMethodInfluentialModularity, working memory, and second language acquisition: A research program
Truscott, J. (2017) · Second language Research · doi:10.1177/0267658317696127 · Cited by 46
“Neural research has found that LTM is functionally fragmented, its visual aspects in visual areas, motor aspects in motor areas, etc. (e.g. Fuster, 2009; Jonides et al., 2008; Rissman and Wagner, 2012).”
BackgroundGoal-directed learning in adolescence: neurocognitive development and contextual influences
Wilbrecht, L., & Davidow, J. Y. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-023-00783-w · Cited by 47
Cortical Representations of Visual Stimuli Shift Locations with Changes in Memory States
Long, N. M., & Kuhl, B. A. (2021) · Current Biology · doi:10.1016/j.cub.2021.01.004 · Cited by 41
Weber, E. M. G., Hahn, T., Hilger, K., & Fiebach, C. J. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.10.006 · Cited by 44
“, 2016) and highlight the importance of using multivariate pattern methods to understand neurocognitive functioning (Mourao-Miranda et al., 2005; Rissman and Wagner, 2012).”
Episodic retrieval involves early and sustained effects of reactivating information from encoding
Johnson, J. D., Price, M. H., & Leiker, E. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.11.013 · Cited by 39
“…as episodes are encoded into memory is reactivated when those memories are retrieved (for reviews, see Rugg et al., 2008; Danker and Anderson, 2010; Rissman and Wagner, 2012), consistent with the notion that successful retrieval depends on hippocampallymediated reinstatement (completion) of…”
Age-related differences in agenda-driven monitoring of format and task information
Mitchell, K., Ankudowich, E., Durbin, K. A., Greene, E. J., & Johnson, M. K. (2013) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2013.01.012 · Cited by 42
“In addition, consistent with the context reinstatement hypothesis (Tulving and Thomson, 1973), the extent to which this activity (or pattern of activity) is recapitulated at test is related to episodic memory accuracy (see Rissman and Wagner (2012) for a review).”
Memory and Self–Neuroscientific Landscapes
Markowitsch, H. J. (2013) · ISRN Neuroscience · doi:10.1155/2013/176027 · Cited by 43
“We still have only begun to unravel the brain processes responsible for memory consolidation [413–416], storage, and retrieval [242, 417, 418].”
BackgroundClark, I. A., Niehaus, K. E., Duff, E. P., Di Simplicio, M. C., Clifford, G. D., Smith, S. M., Mackay, C. E., Woolrich, M. W., & Holmes, E. A. (2014) · Behaviour Research and Therapy · doi:10.1016/j.brat.2014.07.010 · Cited by 37
The real epistemic significance of perceptual learning
Brogaard, B., & Gatzia, D. (2017) · Inquiry · doi:10.1080/0020174x.2017.1368172 · Cited by 20
ACC Theta Improves Hippocampal Contextual Processing during Remote Recall
Wirt, R. A., & Hyman, J. M. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.080 · Cited by 41
“Memories are thought to be stored as a loose connection of distributed networks spread out in many brain regions, with individual features reliant on different areas (Mishkin, 1982; Rissman and Wagner, 2012).”
BackgroundReinstatement of Event Details during Episodic Simulation in the Hippocampus
Thakral, P. P., Madore, K. P., Addis, D. R., & Schacter, D. L. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz242 · Cited by 35
Bonnici, H. M., Sidhu, M. K., Chadwick, M. J., Duncan, J. S., & Maguire, E. A. (2013) · Epilepsy Research · doi:10.1016/j.eplepsyres.2013.01.004 · Cited by 36
Decoding Task-based Attentional Modulation during Face Categorization
Chiu, Y., Esterman, M. S., Han, Y., Rosen, H., & Yantis, S. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21503 · Cited by 36
Westphal, A. J., Reggente, N., Ito, K. L., & Rissman, J. (2015) · Human Brain Mapping · doi:10.1002/hbm.23074 · Cited by 36
“To the degree that overlapping RLPFC activations are observed across the memory and reasoning tasks, we can use multivariate classification techniques [Rissman and Wagner, 2012; Tong and Pratte, 2012] to examine whether the underlying BOLD activity patterns nonetheless contain subtle markers of task-set identity, indi…”
MethodSelf-citationNeural specificity of scene representations is related to memory performance in childhood
Fandakova, Y., Leckey, S., Driver, C., Bunge, S. A., & Ghetti, S. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.05.050 · Cited by 35
Hierarchical nonlinear dynamics of human attention
Rabinovich, M. I., Tristan, I., & Varona, P. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.001 · Cited by 38
Substantial SNP-based heritability estimates for working memory performance
Vogler, C., Gschwind, L., Coynel, D., Freytag, V., Milnik, A., Egli, T., Heck, A., de Quervain, D. J. ‐., & Papassotiropoulos, A. (2014) · Translational Psychiatry · doi:10.1038/tp.2014.81 · Cited by 35
Schyns, P. G., Zhan, J., Jack, R. E., & Ince, R. A. A. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0705 · Cited by 33
Metadata
- Authors
- Rissman, J., & Wagner, A. D.
- Affiliations
- University of California, Los Angeles (US)
- Stanford University (US)
- Venue
- Annual Review of Psychology
- Publisher
- Annual Reviews
- Published
- 2012-01-10
- Volume
- 63
- Issue
- 1
- Pages
- 101-128
- ISSN
- 0066-4308 (ISSN-L)
- 1545-2085
- PMC
- PMC4533899
- OpenAlex
- W2141815738
- Cited by
- 299
- References
- 179
- Citations by year
- 2026: 10 · 2025: 16 · 2024: 19 · 2023: 14 · 2022: 17 · 2021: 29 · 2020: 11 · 2019: 20 · 2018: 23 · 2017: 27 · 2016: 17 · 2015: 28 · 2014: 17 · 2013: 19 · 2012: 13
- FWCI
- 1.41
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Annual Review of Psychology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (5r01mh080309-04)
- National Institute of Mental Health (R01-MH080309, 5R01MH080309, R01MH076932)
- National Institute of Neurological Disorders and Stroke (F32NS059195)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Keywords
- distributed representations, memory, neuronal ensembles, multi-voxel pattern analysis, memory-guided behavior, memory encoding, memory retrieval, perceptual content, semantic content, memory theory, functional MRI
- MeSH terms
- Brain, Brain Mapping, Humans, Memory, Short-Term, Functional Neuroimaging, Memory, Episodic
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