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Episodic and associative memory from spatial scaffolds in the hippocampus

Abstract

Hippocampal circuits in the brain enable two distinct cognitive functions: the construction of spatial maps for navigation, and the storage of sequential episodic memories1,2,3,4,5. Although there have been advances in modelling spatial representations in the hippocampus6,7,8,9,10, we lack good models of its role in episodic memory. Here we present a neocortical–entorhinal–hippocampal network model that implements a high-capacity general associative memory, spatial memory and episodic memory. By factoring content storage from the dynamics of generating error-correcting stable states, the circuit (which we call vector hippocampal scaffolded heteroassociative memory (Vector-HaSH)) avoids the memory cliff of prior memory models11,12, and instead exhibits a graceful trade-off between number of stored items and recall detail. A pre-structured internal scaffold based on grid cell states is essential for constructing even non-spatial episodic memory: it enables high-capacity sequence memorization by abstracting the chaining problem into one of learning low-dimensional transitions. Vector-HaSH reproduces several hippocampal experiments on spatial mapping and context-based representations, and provides a circuit model of the ‘memory palaces’ used by memory athletes13. Thus, this work provides a unified understanding of the spatial mapping and associative and episodic memory roles of the hippocampus.

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Fig. 1: Biological memory: challenges and proposed architecture.
Fig. 2: The scaffold generates exponentially many attractors with equally large basins.
Fig. 3: High-capacity content-addressable item memory via heteroassociation with scaffold.
Fig. 4: Memory, inference and lifelong learning in the spatial domain.
Fig. 5: Sequence scaffold with low-dimensional grid cell shifts enables high-capacity episodic (sequence) memory.
Fig. 6: Vector-HaSH reproduces multiple aspects of entorhinal and hippocampal phenomenology.
Fig. 7: Accurate recall of arbitrary inputs by heteroassociation onto landmarks in a memory palace formed by Vector-HaSH.

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Data availability

Data were collecting by running the codes available at https://github.com/FieteLab.

Code availability

Codes used to run the model and analyse data are available at https://github.com/FieteLab.

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Acknowledgements

This work was supported by ONR award N00014-19-1-2584, by NSF-CISE award IIS-2151077 under the Robust Intelligence programme, by the ARO-MURI award W911NF-23-1-0277, by the Simons Foundation SCGB programme 1181110, and the K. Lisa Yang ICoN Center.

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Contributions

Conceptualization: S.C., S.S., R.C. and I.F. Funding acquisition: I.F. Writing: S.C., S.S. and I.F. Coding and analysis: S.C. and S.S.

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Correspondence to Ila Fiete.

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Extended data figures and tables

Extended Data Fig. 1 Critical number of hippocampal cells necessary to support all scaffold fixed points is asymptotically independent of the number of grid cells.

For a given number of modules, the critical number of hippocampal cells, \({N}_{h}^{* }\) increases slowly with the number of grid cells, but then asymptotically approaches a constant, as expected from the theoretical results in Sec. C.1.

Extended Data Fig. 2 Learning generalization approaches theoretical expectations with increasing Nh.

The number of generated fixed points approaches the maximal scaffold capacity for a very small number of learned patterns (see also Fig. 2f). As the number of hippocampal cells increases, the number of learning patterns necessary for complete generalization approaches the theoretical expectation of M × Kmax, as proved in SI Sec. C.4.

Extended Data Fig. 3 Hebbian learning between sensory layer and scaffold also produces memory continuum.

A memory continuum is obtained in Vector-HaSH even if the weights between the sensory and hippocampal layers are bi-directionally trained using Hebbian learning (instead of pseudoinverse learning, as in Fig. 3. This continuum is also asymptotically proportional to the theoretical bound on memory capacity (forest green dashed line indicative of slope of theoretical upper bound, vertical and horizontal position of dashed line is arbitrary). However, the proportionality constant is lower, with the gradual degradation of information recall occurring well before Nh. Vector-HaSH parameters identical to Fig. 3c with λ = {3, 4, 5}.

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Chandra, S., Sharma, S., Chaudhuri, R. et al. Episodic and associative memory from spatial scaffolds in the hippocampus. Nature 638, 739–751 (2025). https://doi.org/10.1038/s41586-024-08392-y

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