Nathan Schultheiss,
Tomas Guilarte,
Tim AllenNeurostars discussion linkDelta-frequency activity in the local field potential (LFP) is widely believed to correspond to so-called 'cortical silence' during phases of non-REM sleep, but delta in awake behaving animals is not well understood and is rarely studied in detail. By integrating novel analyses of the hippocampal (HC) LFP with simultaneous behavioral tracking, we show for the first time that HC synchronization in the delta frequency band (1-4 Hz) is related to animals' locomotor behaviors during free exploration and foraging in an open field environment. In contrast to well-established relationships between animals' running speeds and the theta rhythm (6-10 Hz), we found that delta was most prominent when animals were stationary or moving slowly (i.e. when theta and fast gamma (65-120 Hz) were weak). Furthermore, delta synchronization often developed rapidly when animals paused briefly between intermittent running bouts.
Next, we developed an innovative strategy for identifying putative _modes_ of network function based on the spectral content of the LFP. By applying hierarchical clustering algorithms to time-windowed power spectra throughout behavioral sessions (i.e. the spectrogram), we categorized moment-by-moment estimations of the power spectral density (PSD) into spectral modes of HC activity. That is, we operationalized putative _functional modes_ of network computation as _spectral modes_ of LFP activity. Delta and theta power were strikingly orthogonal across the resultant spectral modes, suggesting the possibility that delta- and theta-dominated hippocampal activity patterns represent distinct modes of HC function during navigation. Delta and theta were also remarkably orthogonal across precisely-defined bouts of running and stationary behavior, indicating that the stops-and-starts that compose rats' locomotor trajectories are accompanied by alternating delta- and theta-dominated HC states.
We then asked whether the incidence of delta and theta modes was related to the coherence between recording sites in hippocampus or between hippocampus and medial prefrontal cortex (mPFC). We found that intrahippocampal coherences in both the delta-band and the theta-band were monotonically related to theta-delta ratios across modes. Furthermore, in two rats implanted with dual-site recording arrays, we found that theta coherence between HC and mPFC increased during running, and delta-band coherence between mPFC and HC increased during stationary bouts. Taken together, our findings suggest that delta-dominated network modes (and corresponding mPFC-HC couplings) represent functionally-distinct circuit dynamics that are temporally and behaviorally interspersed among theta-dominated modes during spatial navigation. As such, delta modes could play a fundamental role in coordinating mnemonic functions including encoding and retrieval mechanisms, or decision-making processes incorporating prospective or retrospective representations of experience, at a timescale that segments event sequences within behavioral episodes.
