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Conjunctive spatial and self-motion codes are topographically organized in the GABAergic cells of the lateral septum

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  • Suzanne van der Veldt
  • Guillaume Etter
  • Coralie-Anne Mosser
  • Frédéric Manseau
  • Sylvain Williams

Abstract

The hippocampal spatial code’s relevance for downstream neuronal populations—particularly its major subcortical output the lateral septum (LS)—is still poorly understood. Here, using calcium imaging combined with unbiased analytical methods, we functionally characterized and compared the spatial tuning of LS GABAergic cells to those of dorsal CA3 and CA1 cells. We identified a significant number of LS cells that are modulated by place, speed, acceleration, and direction, as well as conjunctions of these properties, directly comparable to hippocampal CA1 and CA3 spatially modulated cells. Interestingly, Bayesian decoding of position based on LS spatial cells reflected the animal’s location as accurately as decoding using the activity of hippocampal pyramidal cells. A portion of LS cells showed stable spatial codes over the course of multiple days, potentially reflecting long-term episodic memory. The distributions of cells exhibiting these properties formed gradients along the anterior–posterior and dorsal–ventral axes of the LS, directly reflecting the topographical organization of hippocampal inputs to the LS. Finally, we show using transsynaptic tracing that LS neurons receiving CA3 and CA1 excitatory input send projections to the hypothalamus and medial septum, regions that are not targeted directly by principal cells of the dorsal hippocampus. Together, our findings demonstrate that the LS accurately and robustly represents spatial, directional as well as self-motion information and is uniquely positioned to relay this information from the hippocampus to its downstream regions, thus occupying a key position within a distributed spatial memory network.Calcium imaging of neurons in freely behaving mice reveals how the lateral septum, the main output of the hippocampal place cells, effectively represents information about not only location, but also head direction and self-movement, and may be pivotal in sending this information to downstream brain regions.

Suggested Citation

  • Suzanne van der Veldt & Guillaume Etter & Coralie-Anne Mosser & Frédéric Manseau & Sylvain Williams, 2021. "Conjunctive spatial and self-motion codes are topographically organized in the GABAergic cells of the lateral septum," PLOS Biology, Public Library of Science, vol. 19(8), pages 1-36, August.
  • Handle: RePEc:plo:pbio00:3001383
    DOI: 10.1371/journal.pbio.3001383
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    Cited by:

    1. Solomiia Korchynska & Patrick Rebernik & Marko Pende & Laura Boi & Alán Alpár & Ramon Tasan & Klaus Becker & Kira Balueva & Saiedeh Saghafi & Peer Wulff & Tamas L. Horvath & Gilberto Fisone & Hans-Ulr, 2022. "A hypothalamic dopamine locus for psychostimulant-induced hyperlocomotion in mice," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Guillaume Etter & Suzanne Veldt & Jisoo Choi & Sylvain Williams, 2023. "Optogenetic frequency scrambling of hippocampal theta oscillations dissociates working memory retrieval from hippocampal spatiotemporal codes," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    3. Daniel Müller-Komorowska & Baris Kuru & Heinz Beck & Oliver Braganza, 2023. "Phase information is conserved in sparse, synchronous population-rate-codes via phase-to-rate recoding," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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