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A unifying perspective on neural manifolds and circuits for cognition

Abstract

Two different perspectives have informed efforts to explain the link between the brain and behaviour. One approach seeks to identify neural circuit elements that carry out specific functions, emphasizing connectivity between neurons as a substrate for neural computations. Another approach centres on neural manifolds — low-dimensional representations of behavioural signals in neural population activity — and suggests that neural computations are realized by emergent dynamics. Although manifolds reveal an interpretable structure in heterogeneous neuronal activity, finding the corresponding structure in connectivity remains a challenge. We highlight examples in which establishing the correspondence between low-dimensional activity and connectivity has been possible, unifying the neural manifold and circuit perspectives. This relationship is conspicuous in systems in which the geometry of neural responses mirrors their spatial layout in the brain, such as the fly navigational system. Furthermore, we describe evidence that, in systems in which neural responses are heterogeneous, the circuit comprises interactions between activity patterns on the manifold via low-rank connectivity. We suggest that unifying the manifold and circuit approaches is important if we are to be able to causally test theories about the neural computations that underlie behaviour.

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Fig. 1: Convergence of a manifold and circuit in the head direction system.
Fig. 2: Manifolds and circuits for spatial position encoding.
Fig. 3: Low-dimensional task manifolds in heterogeneous responses of cortical neurons.

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Acknowledgements

This work was supported by the Swartz Foundation (C.L. and M.G.), National Institutes of Health (NIH) grant R01 EB026949 (T.A.E. and M.G.), NIH grant RF1DA055666 (T.A.E., C.L. and M.G.) and Alfred P. Sloan Foundation Research Fellowship (T.A.E.).

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Langdon, C., Genkin, M. & Engel, T.A. A unifying perspective on neural manifolds and circuits for cognition. Nat Rev Neurosci 24, 363–377 (2023). https://doi.org/10.1038/s41583-023-00693-x

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