STABLE AND UNSTABLE PLACE CELLS EXHIBIT DISTINCT THETA-PHASE DYNAMICS IN HIPPOCAMPAL CA1 AREA

Hippocampal place cells encode spatial information through both spike rate and spike timing relative to the theta phase, reflecting rate and temporal coding mechanisms in the hippocampus. In the CA1 area of hippocampus, neuronal activation at theta frequencies optimally induces long-term synaptic potentiation and supports stable place field representations. However, a substantial fraction of place cells exhibits unstable spatial tuning, and the relationship between rate and temporal coding, as well as the functional significance of this instability, remain unclear.
Here, we compare the firing properties and theta-phase relationships of stable and unstable place-modulated pyramidal neurons in CA1. We performed recordings of neuronal activity using Neuropixels silicon probes in freely behaving mice (n = 7) during a 30-minute open-field session.
Unstable place-tuned neurons exhibited significantly lower firing rates and distinct firing dynamics during novel environment exploration. Stable neurons formed larger place fields, exhibited higher peak firing rates, and carried greater spatial information. In contrast, unstable neurons showed a reduced size of high-rate zones within place fields. Theta-phase locking revealed a systematic phase shift between the two populations: stable neurons tended to fire closer to the ascending phase of theta, whereas unstable neurons were biased toward the descending phase. Differences in theta-phase relationships and place field structure were accompanied by altered phase precession in unstable neurons.
These findings indicate that spatial instability in CA1 reflects a distinct firing and theta-phase-organized regime, potentially supporting flexible spatial representations.
We gratefully acknowledge support by the DFG CRC1451 (to TK and AS).