From movement to cognitive maps: recurrent neural networks reveal how locomotor development shapes hippocampal spatial coding

Abrate, M. P.; Muessig, L.; Cacucci, F.; Bassett, J. P.; Tan, H. M.; Wills, T. J.; Barry, C.

doi:10.64898/2025.12.30.696864

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bioRxiv · 10.64898/2025.12.30.696864

From movement to cognitive maps: recurrent neural networks reveal how locomotor development shapes hippocampal spatial coding

Abrate, M. P.·Muessig, L.·Cacucci, F.·Bassett, J. P.·Tan, H. M.·Wills, T. J.·Barry, C.

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Abstract

AO_SCPLOWBSTRACTC_SCPLOWThe hippocampus contains neurons whose firing correlates with an animals location and orientation in space. Collectively, these neurons are held to support a cognitive map of the environment, enabling the recall of and navigation to specific locations. Although recent studies have characterised the timelines of spatial neuron development, no unifying mechanistic model has yet been proposed. Moreover, the processes driving the emergence of spatial representations in the hippocampus remain unclear (Tan et al., 2017). Here, we combine computational analysis of postnatal locomotor development with a recurrent neural network (RNN) model of hippocampal function to demonstrate how changes in movement statistics - and the resulting sensory experiences - shape the formation of spatial tuning. First, we identify distinct developmental stages in rat locomotion during open-field exploration using published experimental data. Then, we train shallow RNNs to predict upcoming visual stimuli from concurrent visual and vestibular inputs, exposing them to trajectories that reflect progressively maturing locomotor patterns. Our findings reveal that these changing movement statistics drive the sequential emergence of spatially tuned units, mirroring the developmental timeline observed in rats. The models generate testable predictions about how spatial tuning properties mature - predictions we confirm through analysis of hippocampal recordings. Critically, we demonstrate that replicating the specific statistics of developmental locomotion - rather than merely accelerating sensory change - is essential for the emergence of an allocentric spatial representation. These results establish a mechanistic link between embodied sensorimotor experience and the ontogeny of hippocampal spatial neurons, with significant implications for neurodevelopmental research and predictive models of navigational brain circuits.*

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Abrate, M. P., Muessig, L., Cacucci, F., Bassett, J. P., Tan, H. M., Wills, T. J., Barry, C.. 2025-12-30. From movement to cognitive maps: recurrent neural networks reveal how locomotor development shapes hippocampal spatial coding. https://doi.org/10.64898/2025.12.30.696864

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