Binding of Episodic Memories in the Rat
Open accessAbstract
People remember an event as a coherent scene. Memory of such an episode is thought to reflect binding of a fully integrated representation, rather than memory of unconnected features. However, it is not known whether rodents form bound representations. Here we show that rats remember episodes as bound representations. Rats were presented with multiple features of unique episodes at memory encoding: what (food flavor), where (maze location), source (self-generated food seeking—running to the food site—or experimenter-generated food seeking—placement by the experimenter at the food site), and context (spatial cues in the room where the event occurred). After a delay, the trial continued with a memory assessment in which one flavor replenished at the self-generated—but not at experimenter-generated—locations. We presented rats with multiple overlapping features, in rapid succession, to ensure that successful memory retrieval required them to disambiguate multiple study episodes (using two rooms). We found that binding is resistant to interference from highly similar episodes and survives long retention intervals (∼1 week). Our results suggest that multiple episodic memories are each structured as bound representations, which suggests that nonhumans represent episodic memories using a structure similar to that of people. This finding enhances the translational potential for utilizing animal models of episodic memory to explore the biological mechanisms of memory and validate therapeutic approaches for treating disorders of memory.
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Studies using the what-where-when paradigm predominantly focus on the content criterion, and there is little evidence for the structure and flexibility criteria in the literature.
“these predominantly focus on the content criterion, and as a result, there is little evidence for the structure (but see [68,75]) and flexibility (but see [74]) criteria in the literature.”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [68]
The same binding of multiple event features, permitting discrimination between two similar events, has also been demonstrated in rats and apes.
“The same binding of multiple event features, permitting the discrimination between two similar events, has also been demonstrated in rats and apes [68,75].”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [68]
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Cites
(1983) · Medical Entomology and Zoology · Cited by 6,051 · see citing works
Johnson, M. K., Hashtroudi, S., & Lindsay, D. S. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.114.1.3 · Cited by 3,392 · see citing works
The Medial Temporal Lobe and Recognition Memory
Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094328 · Cited by 2,580 · see citing works
Episodic-like memory during cache recovery by scrub jays
Clayton, N. S., & Dickinson, A. (1998) · Nature · doi:10.1038/26216 · Cited by 1,464 · see citing works
A purely geometric module in the rat's spatial representation
Cheng, K. (1986) · Cognition · doi:10.1016/0010-0277(86)90041-7 · Cited by 1,182 · see citing works
Feature memory and binding in young and older adults
Chalfonte, B. L., & Johnson, M. K. (1996) · Memory & Cognition · doi:10.3758/bf03200930 · Cited by 835 · see citing works
Organizational effects of early gonadal secretions on sexual differentiation in spatial memory.
Williams, C. L., Barnett, A. M., & Meck, W. H. (1990) · Behavioral Neuroscience · doi:10.1037//0735-7044.104.1.84 · Cited by 486 · see citing works
Stimulus control of spatial behavior on the eight-arm maze in rats
Suzuki, S., Augerinos, G., & Black, A. H. (1980) · Learning and Motivation · doi:10.1016/0023-9690(80)90018-1 · Cited by 485 · see citing works
Organizational effects of early gonadal secretions on sexual differentiation in spatial memory.
Williams, C. L., Barnett, A. M., & Meck, W. H. (1990) · Behavioral Neuroscience · doi:10.1037/0735-7044.104.1.84 · Cited by 417 · see citing works
Hippocampal spatial representations require vestibular input
Stackman, R. W., Clark, A. S., & Taube, J. S. (2002) · Hippocampus · doi:10.1002/hipo.1112 · Cited by 383 · see citing works
Roskies, A. L. (1999) · Neuron · doi:10.1016/s0896-6273(00)80817-x · Cited by 334 · see citing works
Mental time travel in animals?
Suddendorf, T., & Grant, J. B. (2003) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(03)00187-6 · Cited by 329 · see citing works
Episodic-like Memory in the Rat
Babb, S. J., & Crystal, J. D. (2006) · Current Biology · doi:10.1016/j.cub.2006.05.025 · Cited by 308 · see citing works
Self-citationHippocampal mechanisms for the context-dependent retrieval of episodes
Hasselmo, M. E., & Eichenbaum, H. (2005) · Neural Networks · doi:10.1016/j.neunet.2005.08.007 · Cited by 298 · see citing works
The Hippocampus and Memory for “What,” “Where,” and “When”
Ergorul, C., & Eichenbaum, H. (2004) · Learning & Memory · doi:10.1101/lm.73304 · Cited by 294 · see citing works
Medial Temporal Lobe Activity Predicts Successful Relational Memory Binding
Hannula, D. E., & Ranganath, C. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3086-07.2008 · Cited by 280 · see citing works
Keeping track of time: evidence for episodic-like memory in great apes
Martin-Ordas, G., Haun, D., Colmenares, F., & Call, J. (2010) · Animal Cognition · doi:10.1007/s10071-009-0282-4 · Cited by 244 · see citing works
Clayton, N. S., Yu, K. S., & Dickinson, A. (2001) · Journal of Experimental Psychology: Animal Behavior Processes · doi:10.1037//0097-7403.27.1.17 · Cited by 238 · see citing works
Theta Oscillations at Encoding Mediate the Context-Dependent Nature of Human Episodic Memory
Staudigl, T., & Hanslmayr, S. (2013) · Current Biology · doi:10.1016/j.cub.2013.04.074 · Cited by 225 · see citing works
Intramaze cues and “odor trails” fail to direct choice behavior on an elevated maze
Olton, D. S., & Collison, C. (1979) · Animal Learning & Behavior · doi:10.3758/bf03209274 · Cited by 204 · see citing works
Episodic-like memory in rats: is it based on when or how long ago?
Roberts, W. A., Feeney, M. C., MacPherson, K., Petter, M., McMillan, N., & Musolino, E. (2008) · Science · doi:10.1126/science.1152709 · Cited by 191 · see citing works
Discrimination of what, when, and where: Implications for episodic-like memory in rats
Babb, S. J., & Crystal, J. D. (2005) · Learning and Motivation · doi:10.1016/j.lmot.2005.02.009 · Cited by 181 · see citing works
Self-citationRecollection in an episodic-like memory task in the rat
Eacott, M. J., Easton, A., & Zinkivskay, A. (2005) · Learning & Memory · doi:10.1101/lm.92505 · Cited by 164 · see citing works
The vestibular contribution to the head direction signal and navigation
Yoder, R. M., & Taube, J. S. (2014) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2014.00032 · Cited by 161 · see citing works
Origins of landmark encoding in the brain
Yoder, R. M., Clark, B. J., & Taube, J. S. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.08.004 · Cited by 155 · see citing works
Evidence for remembering when events occurred in a rodent model of episodic memory
Zhou, W., & Crystal, J. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904360106 · Cited by 152 · see citing works
Self-citationDiscrimination of what, when, and where is not based on time of day
Babb, S. J., & Crystal, J. D. (2006) · Learning & Behavior · doi:10.3758/bf03193188 · Cited by 136 · see citing works
Self-citationInfluence of vestibular input on spatial and nonspatial memory and on hippocampal NMDA receptors
Besnard, S., Machado, M., Vignaux, G., Boulouard, M., Coquerel, A., Bouët, V., Fréret, T., Denise, P., & Lelong‐Boulouard, V. (2011) · Hippocampus · doi:10.1002/hipo.20942 · Cited by 123 · see citing works
Ferkin, M. H., Combs, A., delBarco‐Trillo, J., Pierce, A. A., & Franklin, S. (2007) · Animal Cognition · doi:10.1007/s10071-007-0101-8 · Cited by 107 · see citing works
Rats Answer an Unexpected Question after Incidental Encoding
Zhou, W., Hohmann, A. G., & Crystal, J. D. (2012) · Current Biology · doi:10.1016/j.cub.2012.04.040 · Cited by 98 · see citing works
Self-citationBilateral peripheral vestibular lesions produce long-term changes in spatial learning in the rat
Russell, N. A., Horii, A., Smith, P. F., et al. (2003) · Journal of Vestibular Research · doi:10.3233/ves-2003-13102 · Cited by 97 · see citing works
Retroactive inhibition in rat spatial memory
Roberts, W. A. (1981) · Animal Learning & Behavior · doi:10.3758/bf03209792 · Cited by 82 · see citing works
Crystal, J. D., Alford, W. T., Zhou, W., & Hohmann, A. G. (2013) · Current Biology · doi:10.1016/j.cub.2013.01.023 · Cited by 82 · see citing works
Self-citationHierarchical structures: Chunking by food type facilitates spatial memory.
Dallal, N. L., & Meck, W. H. (1990) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.16.1.69 · Cited by 79 · see citing works
Two rooms, two representations? Episodic‐like memory in toddlers and preschoolers
Newcombe, N. S., Balcomb, F. K., Ferrara, K., Hansen, M., & Koski, J. E. (2014) · Developmental Science · doi:10.1111/desc.12162 · Cited by 79 · see citing works
Memory for “what”, “where”, and “when” information in rhesus monkeys (Macaca mulatta).
Hoffman, M. L., Beran, M. J., & Washburn, D. A. (2009) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/a0013295 · Cited by 79 · see citing works
Mental time travel in animals: A challenging question
Zentall, T. R. (2006) · Behavioural Processes · doi:10.1016/j.beproc.2006.01.009 · Cited by 77 · see citing works
Ossenkopp, K., & Hargreaves, E. L. (1993) · Behavioral and Neural Biology · doi:10.1016/0163-1047(93)91034-k · Cited by 72 · see citing works
Associative Representations of Instrumental Contingencies
Colwill, R. (1994) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/s0079-7421(08)60408-9 · Cited by 67 · see citing works
Animals may not be stuck in time
Zentall, T. R. (2005) · Learning and Motivation · doi:10.1016/j.lmot.2005.03.001 · Cited by 62 · see citing works
Validation of a rodent model of episodic memory
Zhou, W., & Crystal, J. D. (2011) · Animal Cognition · doi:10.1007/s10071-010-0367-0 · Cited by 60 · see citing works
Self-citationSpatial memory in rats under restricted viewing conditions
Mazmanian, D. S., & Roberts, W. A. (1983) · Learning and Motivation · doi:10.1016/0023-9690(83)90001-2 · Cited by 57 · see citing works
Spatial guidance of choice behavior in the radial-arm maze.
Brown, M. F., Rish, P. A., VonCulin, J. E., & Edberg, J. A. (1993) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.19.3.195 · Cited by 50 · see citing works
Validation of a rodent model of source memory
Crystal, J. D., & Alford, W. T. (2014) · Biology Letters · doi:10.1098/rsbl.2014.0064 · Cited by 37 · see citing works
Self-citationA biological perspective on memory
Crystal, J. D., & Glanzman, D. L. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.082 · Cited by 21 · see citing works
Self-citationOlthof, A., Sutton, J. E., Slumskie, S. V., et al. (1999) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037//0097-7403.25.3.352 · Cited by 17 · see citing works
Olthof, A., Sutton, J. E., Slumskie, S. V., et al. (1999) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.25.3.352 · Cited by 11 · see citing works
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Replay of Episodic Memories in the Rat
Panoz-Brown, D., Iyer, V., Carey, L. M., Sluka, C. M., Rajic, G., Kestenman, J., Gentry, M., Brotheridge, S., Somekh, I., Corbin, H. E., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.04.006 · Cited by 101 · see citing works
Self-citationAnimal models of episodic memory
Crystal, J. D. (2018) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2018.130012 · Cited by 59 · see citing works
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Sheridan, C. L., Lang, S., Knappenberger, M., Albers, C., Loper, R., Tillett, B., Sanchez, J., Wilcox, A., Harrison, T., Panoz-Brown, D., et al. (2024) · Current Biology · doi:10.1016/j.cub.2023.12.043 · Cited by 40 · see citing works
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Davies, J. R., & Clayton, N. S. (2024) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2023.0397 · Cited by 27 · see citing works
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Auguste, A., Fourcaud-Trocmé, N., Meunier, D., Gros, A., Garcia, S., Messaoudi, B., Thevenet, M., Ravel, N., & Veyrac, A. (2023) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2023.102422 · Cited by 14 · see citing works
- Authors
- Crystal, J. D., & Smith, A. E.
- Affiliations
- Indiana University Bloomington (US)
- Corresponding author
- Crystal, Jonathon D.
- ORCID
- Crystal, Jonathon D.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2014-12
- Volume
- 24
- Issue
- 24
- Pages
- 2957-2961
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC4269559
- OpenAlex
- W1994823121
- Cited by
- 77
- References
- 47
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 14 · 2023: 3 · 2022: 10 · 2021: 4 · 2020: 7 · 2019: 9 · 2018: 5 · 2017: 7 · 2016: 5 · 2015: 2 · 2014: 1
- FWCI
- 2.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation
- National Institutes of Health
- Indiana University Bloomington
- National Institute on Aging (R21AG044530)
- National Institute of Mental Health (R01MH098985)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Keywords
- episodic memory, memory binding, rats, source memory, spatial context, food flavor, memory interference, memory retention, animal models of memory
- MeSH terms
- Animals, Cues, Male, Mental Recall, Taste, Rats, Long-Evans, Rats, Memory, Episodic
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