A population code for idiothetic representations in the hippocampal-septal circuit

Abstract

The hippocampus is a higher-order brain structure responsible for encoding new episodic memories and predicting future outcomes. In absence of external stimuli, neurons in the hippocampus express sequential activities which have been proposed to support path integration by tracking elapsed time, distance traveled, and other idiothetic variables. On the other hand, with sufficient external sensory inputs, hippocampal neurons can fire with respect to allocentric cues. Previously, these idiothetic codes have been described in conditions where running speed is clamped experimentally. To this day, the exact determinants of idiothetic representations during free navigation remain unclear. Additionally, whether CA1 and CA3 temporal and distance codes are transmitted downstream to the lateral septum has not been established. Here, we develop an unsupervised model trained to compress neural information with minimal loss, and find that we can efficiently decode elapsed time and distance traveled from low-dimensional embeddings of neural activity in freely moving mice. We also developed unbiased information metrics that are minimally sensitive to quantization parameters and enable comparisons across modalities and brain regions. In more than 30,000 CA1 pyramidal neurons, we show that spatiotemporal information is represented as a mixture of idiothetic and allocentric information, the balance of which is dictated by task demand and environmental conditions. In particular, we find that a subset of CA1 pyramidal neurons encode the spatiotemporal distance to rewards. Single cell and population statistics across the hippocampal-septal circuit reveal that idiothetic variables emerge in CA1 and are integrated postsynaptically in the lateral septum. Finally, we implement a computational model trained to replicate real world neural activity, and find that grid cells could provide a plausible input for CA1 representations of time and distance. Altogether, our results suggest that hippocampal CA1 continuously integrates both idiothetic and allocentric signals depending on task demand and available cues, and these high-level representations are effectively transmitted to downstream regions.