Learning reshapes the hippocampal representation hierarchy
Chiossi HSC, Nardin M, Tkačik G, Csicsvari JL. 2025. Learning reshapes the hippocampal representation hierarchy. Proceedings of the National Academy of Sciences. 122(11), e2417025122.
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Abstract
A key feature of biological and artificial neural networks is the progressive refinement of their neural representations with experience. In neuroscience, this fact has inspired several recent studies in sensory and motor systems. However, less is known about how higher associational cortical areas, such as the hippocampus, modify representations throughout the learning of complex tasks. Here, we focus on associative learning, a process that requires forming a connection between the representations of different variables for appropriate behavioral response. We trained rats in a space-context associative task and monitored hippocampal neural activity throughout the entire learning period, over several days. This allowed us to assess changes in the representations of context, movement direction, and position, as well as their relationship to behavior. We identified a hierarchical representational structure in the encoding of these three task variables that was preserved throughout learning. Nevertheless, we also observed changes at the lower levels of the hierarchy where context was encoded. These changes were local in neural activity space and restricted to physical positions where context identification was necessary for correct decision-making, supporting better context decoding and contextual code compression. Our results demonstrate that the hippocampal code not only accommodates hierarchical relationships between different variables but also enables efficient learning through minimal changes in neural activity space. Beyond the hippocampus, our work reveals a representation learning mechanism that might be implemented in other biological and artificial networks performing similar tasks.
Publishing Year
Date Published
2025-03-10
Journal Title
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Acknowledgement
We would like to thank Rebecca Morse for performing the recordings in one of the animals under the supervision of H.S.C.C., Jago Wallenschus for the technical support, especially with maze design, Wiktor Mlynarski for the advice and discussions and Andrea Cumpelik for suggestions during the writing. M.N. was supported by the Howard Hughes Medical Institute. H.S.C.C. received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 665385.
Volume
122
Issue
11
Article Number
e2417025122
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eISSN
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Cite this
Chiossi HSC, Nardin M, Tkačik G, Csicsvari JL. Learning reshapes the hippocampal representation hierarchy. Proceedings of the National Academy of Sciences. 2025;122(11). doi:10.1073/pnas.2417025122
Chiossi, H. S. C., Nardin, M., Tkačik, G., & Csicsvari, J. L. (2025). Learning reshapes the hippocampal representation hierarchy. Proceedings of the National Academy of Sciences. National Academy of Sciences. https://doi.org/10.1073/pnas.2417025122
Chiossi, Heloisa S. C., Michele Nardin, Gašper Tkačik, and Jozsef L Csicsvari. “Learning Reshapes the Hippocampal Representation Hierarchy.” Proceedings of the National Academy of Sciences. National Academy of Sciences, 2025. https://doi.org/10.1073/pnas.2417025122.
H. S. C. Chiossi, M. Nardin, G. Tkačik, and J. L. Csicsvari, “Learning reshapes the hippocampal representation hierarchy,” Proceedings of the National Academy of Sciences, vol. 122, no. 11. National Academy of Sciences, 2025.
Chiossi HSC, Nardin M, Tkačik G, Csicsvari JL. 2025. Learning reshapes the hippocampal representation hierarchy. Proceedings of the National Academy of Sciences. 122(11), e2417025122.
Chiossi, Heloisa S. C., et al. “Learning Reshapes the Hippocampal Representation Hierarchy.” Proceedings of the National Academy of Sciences, vol. 122, no. 11, e2417025122, National Academy of Sciences, 2025, doi:10.1073/pnas.2417025122.
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