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Abstract representations emerge in human hippocampal neurons during inference.

ABSTRACT: Humans have the remarkable cognitive capacity to rapidly adapt to changing environments. Central to this capacity is the ability to form high-level, abstract representations that take advantage of regularities in the world to support generalization¹. However, little is known about how these representations are encoded in populations of neurons, how they emerge through learning and how they relate to behaviour^2,3. Here we characterized the representational geometry of populations of neurons (single units) recorded in the hippocampus, amygdala, medial frontal cortex and ventral temporal cortex of neurosurgical patients performing an inferential reasoning task. We found that only the neural representations formed in the hippocampus simultaneously encode several task variables in an abstract, or disentangled, format. This representational geometry is uniquely observed after patients learn to perform inference, and consists of disentangled directly observable and discovered latent task variables. Learning to perform inference by trial and error or through verbal instructions led to the formation of hippocampal representations with similar geometric properties. The observed relation between representational format and inference behaviour suggests that abstract and disentangled representational geometries are important for complex cognition.

SUBMITTER: Courellis HS

PROVIDER: S-EPMC11338822 | biostudies-literature | 2024 Aug

REPOSITORIES: biostudies-literature

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Abstract representations emerge in human hippocampal neurons during inference.

Courellis Hristos S HS Minxha Juri J Cardenas Araceli R AR Kimmel Daniel L DL Reed Chrystal M CM Valiante Taufik A TA Salzman C Daniel CD Mamelak Adam N AN Fusi Stefano S Rutishauser Ueli U

Nature 20240814 8026

Humans have the remarkable cognitive capacity to rapidly adapt to changing environments. Central to this capacity is the ability to form high-level, abstract representations that take advantage of regularities in the world to support generalization<sup>1</sup>. However, little is known about how these representations are encoded in populations of neurons, how they emerge through learning and how they relate to behaviour<sup>2,3</sup>. Here we characterized the representational geometry of popula ...[more]

PMID: 39143207

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Project description:The striatum and hippocampus are widely held to be components of distinct memory systems that can guide competing behavioral strategies. However, some electrophysiological studies have suggested that neurons in both structures encode spatial information and may therefore make similar contributions to behavior. In rats well trained to perform a win-stay radial maze task, we recorded simultaneously from dorsal hippocampus and from multiple striatal subregions, including both lateral areas implicated in motor responses to cues and medial areas that work cooperatively with hippocampus in cognitive operations. In each brain region, movement through the maze was accompanied by the continuous sequential activation of sets of projection neurons. Hippocampal neurons overwhelmingly were active at a single spatial location (place cells). Striatal projection neurons were active at discrete points within the progression of every trial-especially during choices or following reward delivery-regardless of spatial position. Place-cell-type firing was not observed even for medial striatal cells entrained to the hippocampal theta rhythm. We also examined neural coding in earlier training sessions, when rats made use of spatial working memory to guide choices, and again found that striatal cells did not show place-cell-type firing. Prospective or retrospective encoding of trajectory was not observed in either hippocampus or striatum, at either training stage. Our results indicate that, at least in this task, dorsal hippocampus uses a spatial foundation for information processing that is not substantially modulated by spatial working memory demands. By contrast, striatal cells do not use such a spatial foundation, even in medial subregions that cooperate with hippocampus in the selection of spatial strategies. The progressive dominance of a striatum-dependent strategy does not appear to be accompanied by large changes in striatal or hippocampal single-cell representations, suggesting that the conflict between strategies may be resolved elsewhere.

Dataset Information

Abstract representations emerge in human hippocampal neurons during inference.

Publications

Abstract representations emerge in human hippocampal neurons during inference.

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