Frequency-specific theta states in the hippocampus modulate population activity with respect to behavioural context

Abstract

Neural activity reflects both external stimuli and the brains internal state, which shapes how information is processed and perceived. An example of modulation of neural responses by network states is phase-precession in the hippocampus, where the phase of theta oscillations affects the firing of single neurons (place cells) and its relation to the external world. Here, we examine a different form of relationship between oscillations and neural activity, where frequency and power of the oscillation, instead of phase, are associated with differential neural firing patterns at the population level. We refer to this as ensemble pattern reconfiguration. To study this effect, we use electrophysiological recordings of rats performing an odour-memory (non-spatial) task. Using a data-driven model, we identified two distinct theta states: low-power-lower-theta (LPLT) and high-power-higher-theta (HPHT). Through regression and decoding analyses, we found that these states are associated to modulations in hippocampal neural ensemble activity representing trial outcome - though the effect did not consistently reach statistical significance in all our subjects. Our findings suggest that power and frequency variations within theta oscillations may be linked to the reconfiguration of neural firing at the network level, motivating further investigation in larger datasets.