The hippocampal memory indexing theory.
Abstract
The hippocampal formation (comprising the hippocampus proper, the dentate gyrus, and the subiculum) has been repeatedly implicated in information storage models of the mammalian brain. The precise nature of the hippocampal role in the storage of information has, however, remained elusive. Here it is proposed that the role of the hippocampus is to form and retain an index of neocortical areas activated by experiential events. The hippocampal index, thus, represents those unique cortical regions activated by specific events. The neuronal mechanism underlying the memory index is hypothesized to be long-term potentiation. It is asserted that the reactivation of the stored hippocampal memory index will serve to also reactivate the associated unique array of neocortical areas and thus will result in a memorial experience. This hippocampal reactivation of a neocortical array may also be involved in establishing a cortically based memory trace.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Different theories on the role of the hippocampus in memory processing have in common the idea that the hippocampus generates a higher-order representation of the contextual components of a learning experience.
“Thus, the different theories on the role of the hippocampus in memory processing have in common the idea that the hippocampus generates a higher-order representation of the contextual components of a learning experience (Teyler and DiScenna [308]; Eichenbaum [309]; O'Reilly and Rudy [306]; Brassen et al. [310]).”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Teyler and DiScenna [308]
Teyler and Discenna propose that human long-term memory relies on interactions between the neocortex and the hippocampus.
“Teyler and Discenna [75] propose that human long-term memory is composed of three components that work together to accomplish two main objectives: pattern separation , which ensures that the representations of distinct perceptual experiences are unique, and pattern completion , which enables the retrieval of complete memories from partial stimuli [19, 76].”
From HippoRAG: Neurobiologically Inspired Long-Term Memory for Large Language Models (2024) · cites this paper as [75]
Hippocampal memory indexing theory is a well-established theory of human long-term memory.
“The hippocampal memory indexing theory [75] is a well-established theory that provides a functional description of the components and circuitry involved in human long-term memory.”
From HippoRAG: Neurobiologically Inspired Long-Term Memory for Large Language Models (2024) · cites this paper as [75]
New information can be integrated by changing only the hippocampal index instead of updating neocortical representations.
“Thus, this complex process allows for new information to be integrated by changing only the hippocampal index instead of updating neocortical representations.”
From HippoRAG: Neurobiologically Inspired Long-Term Memory for Large Language Models (2024) · cites this paper as [75]
Pattern separation is primarily accomplished in the memory encoding process, which starts with the neocortex receiving and processing perceptual stimuli into features routed through the parahippocampal regions to be indexed by the hippocampus.
“The theory suggests that pattern separation is primarily accomplished in the memory encoding process, which starts with the neocortex receiving and processing perceptual stimuli into more easily manipulatable, likely higher-level, features, which are then routed through the parahippocampal regions (PHR) to be indexed by the hippocampus.”
From HippoRAG: Neurobiologically Inspired Long-Term Memory for Large Language Models (2024) · cites this paper as [75]
Pattern completion drives the memory retrieval process whenever the hippocampus receives partial perceptual signals from the PHR pipeline.
“After the memory encoding process is completed, pattern completion drives the memory retrieval process whenever the hippocampus receives partial perceptual signals from the PHR pipeline.”
From HippoRAG: Neurobiologically Inspired Long-Term Memory for Large Language Models (2024) · cites this paper as [75]
Episodic memories depend on many brain regions for their creation and persistence.
“First, episodic memories depend on many brain regions for their creation and persistence.”
From Episodic Memory in AI Agents Poses Risks that Should be Studied and Mitigated (2025) · cites this paper as [69]
According to hippocampal indexing theory, an encoding of an episode in the hippocampus serves as an index that points to and binds together representations in the neocortex.
“According to the hippocampal indexing theory [69], an encoding of an episode in the hippocampus serves as a kind of index that points to and binds together representations in the neocortex that form the basis of the episode, such as multimodal sensory representations along with associated emotional and conceptual information [70].”
From Episodic Memory in AI Agents Poses Risks that Should be Studied and Mitigated (2025) · cites this paper as [69]
Cites
Hebb, D. O. (2005) · doi:10.4324/9781410612403 · Cited by 9,825 · see citing works
Simple memory: a theory for archicortex
Marr, D. (1971) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1971.0078 · Cited by 2,771 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376 · see citing works
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250 · see citing works
Path integration and the neural basis of the 'cognitive map'
McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., & Moser, M.-B. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1932 · Cited by 2,024 · see citing works
Memory consolidation, retrograde amnesia and the hippocampal complex
Nadel, L., & Moscovitch, M. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80010-4 · Cited by 1,924 · see citing works
Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning
Buzsáki, G. (2015) · Hippocampus · doi:10.1002/hipo.22488 · Cited by 1,759 · see citing works
Mind-wandering as spontaneous thought: a dynamic framework
Christoff, K., Irving, Z. C., Fox, K. C. R., Spreng, R. N., & Andrews-Hanna, J. R. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.113 · Cited by 1,376 · see citing works
Schemas and Memory Consolidation.
Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., Wood, E. R., Witter, M. P., & Morris, R. G. M. (2007) · Science · doi:10.1126/science.1135935 · Cited by 1,244 · see citing works
Long-axis specialization of the human hippocampus
Poppenk, J., Evensmoen, H. R., Moscovitch, M., & Nadel, L. (2013) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.03.005 · Cited by 1,100 · see citing works
Adult neurogenesis: from precursors to network and physiology
Abrous, D. N., Koehl, M., & Le Moal, M. (2005) · Physiological Reviews · doi:10.1152/physrev.00055.2003 · Cited by 971 · see citing works
Memory processes, brain oscillations and EEG synchronization
Klimesch, W. (1996) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(96)00057-8 · Cited by 923 · see citing works
The hippocampus—what does it do?
Eichenbaum, H., Otto, T., & Cohen, N. J. (1992) · Behavioral and Neural Biology · doi:10.1016/0163-1047(92)90724-i · Cited by 867 · see citing works
Memory and Working-with-Memory: A Component Process Model Based on Modules and Central Systems
Moscovitch, M. (1992) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1992.4.3.257 · Cited by 822 · see citing works
Kudrimoti, H. S., Barnes, C. A., & McNaughton, B. L. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-10-04090.1999 · Cited by 753 · see citing works
Diamond, D. M., Campbell, A. M., Park, C. R., Halonen, J., & Zoladz, P. R. (2007) · Neural Plasticity · doi:10.1155/2007/60803 · Cited by 762 · see citing works
“Thus, the different theories on the role of the hippocampus in memory processing have in common the idea that the hippocampus generates a higher-order representation of the contextual components of a learning experience (Teyler and DiScenna [308]; Eichenbaum [309]; O’Reilly and Rudy [306]; Brassen et al.”
BackgroundSchema-dependent gene activation and memory encoding in neocortex
Tse, D., Takeuchi, T., Kakeyama, M., Kajii, Y., Okuno, H., Tohyama, C., Bito, H., & Morris, R. G. M. (2011) · Science · doi:10.1126/science.1205274 · Cited by 618 · see citing works
Spatial representation in the hippocampal formation: a history
Moser, E. I., Moser, M.-B., & McNaughton, B. L. (2017) · Nature Neuroscience · doi:10.1038/nn.4653 · Cited by 560 · see citing works
Bidirectional switch of the valence associated with a hippocampal contextual memory engram
Redondo, R. L., Kim, J., Arons, A. L., Ramirez, S., Liu, X., & Tonegawa, S. (2014) · Nature · doi:10.1038/nature13725 · Cited by 512 · see citing works
Space and Time: The Hippocampus as a Sequence Generator
Buzsáki, G., & Tingley, D. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.07.006 · Cited by 461 · see citing works
Concept cells: the building blocks of declarative memory functions
Quiroga, R. Q. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3251 · Cited by 472 · see citing works
Memory trace reactivation in hippocampal and neocortical neuronal ensembles
Sutherland, G. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00079-9 · Cited by 384 · see citing works
The hippocampus and related neocortical structures in memory transformation
Sekeres, M. J., Winocur, G., & Moscovitch, M. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.05.006 · Cited by 370 · see citing works
Memory for events and their spatial context: models and experiments
Burgess, N., Becker, S., King, J. A., & O'Keefe, J. (2001) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2001.0948 · Cited by 377 · see citing works
O'Reilly, R. C., & Norman, K. A. (2002) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(02)02005-3 · Cited by 351 · see citing works
Howard, M. W., Fotedar, M. S., Datey, A. V., & Hasselmo, M. E. (2005) · Psychological Review · doi:10.1037/0033-295x.112.1.75 · Cited by 283 · see citing works
Context representations, context functions, and the parahippocampal–hippocampal system
Rudy, J. W. (2009) · Learning & Memory · doi:10.1101/lm.1494409 · Cited by 296 · see citing works
Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval
Watrous, A. J., Tandon, N., Conner, C. R., Pieters, T., & Ekstrom, A. D. (2013) · Nature Neuroscience · doi:10.1038/nn.3315 · Cited by 296 · see citing works
Elements of episodic-like memory in animals.
Clayton, N. S., Griffiths, D. P., Emery, N. J., & Dickinson, A. (2001) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2001.0947 · Cited by 289 · see citing works
Robin, J., & Moscovitch, M. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.07.016 · Cited by 266 · see citing works
Conjunctive representations, the hippocampus, and contextual fear conditioning
RUDY, J. W., & O'REILLY, R. C. (2001) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.1.1.66 · Cited by 247 · 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
The neurobiological foundation of memory retrieval
Frankland, P. W., Josselyn, S. A., & Köhler, S. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0493-1 · Cited by 228 · see citing works
Prediction and memory: A predictive coding account
Barron, H. C., Auksztulewicz, R., & Friston, K. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101821 · Cited by 220 · see citing works
Neurofunctional mechanisms in autism
Waterhouse, L., Fein, D., & Modahl, C. (1996) · Psychological Review · doi:10.1037/0033-295x.103.3.457 · Cited by 218 · see citing works
Buzsáki, G., & Llinás, R. (2017) · Science · doi:10.1126/science.aan8869 · Cited by 175 · see citing works
Attentive scanning behavior drives one-trial potentiation of hippocampal place fields
Monaco, J. D., Rao, G., Roth, E. D., & Knierim, J. J. (2014) · Nature Neuroscience · doi:10.1038/nn.3687 · Cited by 163 · see citing works
Indicators and criteria of consciousness in animals and intelligent machines: an inside-out approach
Pennartz, C. M. A., Farisco, M., & Evers, K. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00025 · Cited by 121 · see citing works
Multiple interacting brain areas underlie successful spatiotemporal memory retrieval in humans
Schedlbauer, A. M., Copara, M. S., Watrous, A. J., & Ekstrom, A. D. (2014) · Scientific Reports · doi:10.1038/srep06431 · Cited by 119 · see citing works
The associative structure of memory for multi-element events.
Horner, A. J., & Burgess, N. (2013) · Journal of Experimental Psychology: General · doi:10.1037/a0033626 · Cited by 109 · see citing works
Organizing memories for generalization in complementary learning systems
Sun, W., Advani, M., Spruston, N., Saxe, A., & Fitzgerald, J. E. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01382-9 · Cited by 103 · see citing works
Do hippocampal pyramidal cells respond to nonspatial stimuli?
O’Keefe, J., & Krupic, J. (2021) · Physiological Reviews · doi:10.1152/physrev.00014.2020 · Cited by 93 · see citing works
Neurophysiology of Remembering
Buzsáki, G., McKenzie, S., & Davachi, L. (2022) · Annual Review of Psychology · doi:10.1146/annurev-psych-021721-110002 · Cited by 84 · see citing works
Sleep spindles track cortical learning patterns for memory consolidation
Petzka, M., Chatburn, A., Charest, I., Balanos, G. M., & Staresina, B. P. (2022) · Current Biology · doi:10.1016/j.cub.2022.04.045 · Cited by 63 · see citing works
Barnett, A. J., Nguyen, M., Spargo, J., Yadav, R., Cohn-Sheehy, B. I., & Ranganath, C. (2024) · Neuron · doi:10.1016/j.neuron.2023.10.010 · Cited by 55 · see citing works
Memory, consciousness and neuroimaging
The American Association for Research into Nervous and Mental Diseases, Schacter, D. L., Buckner, R. L., & Koutstaal, W. (1998) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.1998.0338 · Cited by 48 · see citing works
Butcher, S. P., Hamberger, A., & Morris, R. G. M. (1991) · Experimental Brain Research · doi:10.1007/bf00229829 · Cited by 40 · see citing works
Moscovitch, M., & Gilboa, A. (2022) · Faculty Reviews · doi:10.12703/r/11-33 · Cited by 27 · see citing works
HippoRAG: Neurobiologically Inspired Long-Term Memory for Large Language Models
Gutiérrez, B. J., Shu, Y., Gu, Y., Yasunaga, M., & Su, Y. (2024) · arXiv · doi:10.48550/arxiv.2405.14831 · Cited by 152 · see citing works
“The hippocampal memory indexing theory [58], a well-established theory of human long-term memory, offers one plausible explanation for this remarkable ability.”
InfluentialSelf-Net: Lifelong Learning via Continual Self-Modeling
Mandivarapu, J. K., Camp, B., & Estrada, R. (2020) · Frontiers in Artificial Intelligence · doi:10.3389/frai.2020.00019 · Cited by 14 · see citing works
Elements of episodic memory: insights from artificial agents
Boyle, A., & Blomkvist, A. (2024) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2023.0416 · Cited by 6 · see citing works
Episodic Memory in AI Agents Poses Risks that Should be Studied and Mitigated
DeChant, C. (2025) · 2025 IEEE Conference on Secure and Trustworthy Machine Learning (SaTML) · doi:10.1109/satml64287.2025.00024 · Cited by 5 · see citing works
Damastuti, F. A., Firmansyah, K., Barakbah, A., & Hariadi, M. (2026) · SSRN Electronic Journal · doi:10.2139/ssrn.6536138
- Authors
- Teyler, T. J., & DiScenna, P.
- Venue
- Behavioral Neuroscience
- Published
- 1986
- Volume
- 100
- Issue
- 2
- Pages
- 147-154
- ISSN
- 0735-7044 (ISSN-L)
- 1939-0084
- OpenAlex
- W4238424379
- Cited by
- 871
- References
- 2
- Citations by year
- 2026: 32 · 2025: 43 · 2024: 73 · 2023: 35 · 2022: 28 · 2021: 34 · 2020: 38 · 2019: 54 · 2018: 31 · 2017: 26 · 2016: 20 · 2015: 10 · 2014: 30 · 2013: 17 · 2012: 11
- FWCI
- 8.11
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioral Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (NS 16507)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- hippocampus, memory retrieval
- MeSH terms
- Animals, Association, Brain Mapping, Cats, Cerebral Cortex, Hippocampus, Humans, Limbic System, Memory, Models, Neurological, Neural Pathways, Synaptic Transmission, Psychophysics, Rabbits, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review