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

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 oscillation-to-neuron modulation, where frequency and power of the oscillation, instead of phase, modulate neural firing patterns at the population level. We refer to this as ensemble pattern modulation. 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 decoding analyses, we found that these states differentially modulate hippocampal neural ensemble activity, in this case reflective of the trial outcome. This suggests that amplitude and frequency variations within theta oscillations may reconfigure neural firing at the network level to support distinct cognitive functions. Significance statementThe brains ability to process information flexibly is crucial for adapting to changing environments and cognitive demands. This study sheds light on how brain states, reflected in hippocampal theta oscillations, dynamically influence the activity of neural ensembles. Using a data-driven approach, we identify two distinct theta states--low-power-lower-theta (LPLT) and high-power-higher-theta (HPHT)-- and show that these states enable the same neural population to encode different aspects of information, depending on the cognitive context. This mechanism, which we term ensemble pattern modulation, advances our understanding of how brain states enable adaptive information processing to achieve functional flexibility.