‘Awake delta’ and theta-rhythmic hippocampal network modes during intermittent locomotor behaviors in the rat

Abstract

Delta-frequency network activity is commonly associated with sleep or behavioral disengagement accompanied by a dearth of cortical spiking, but delta in awake behaving animals is not well understood. We show that hippocampal (HC) synchronization in the delta frequency band (1-4 Hz) is related to animals' locomotor behavior using a detailed analysis of simultaneous head-and bodytracking data. In contrast to running-speed modulation of the theta rhythm (6-10 Hz, a critical mechanism in navigation models), we observed that strong delta synchronization occurred when animals were stationary or moving slowly and while theta and fast gamma (55-120 Hz) were weak. We next combined time-frequency decomposition of the local field potential with hierarchical clustering algorithms to categorize momentary estimations of the power spectral density (PSD) into putative modes of HC activity. Delta and theta power measures from these modes were notably orthogonal, and theta and delta coherences between HC recording sites were monotonically related to theta-delta ratios across modes. Next, we focused on bouts of precisely-defined running and stationary behavior. Extraction of delta and theta power density estimates for each instance of these bout types confirmed the orthogonality between frequency bands seen across modes. We found that delta-band and thetaband coherence within HC, and in a small sample, between HC and medial prefrontal cortex (mPFC), mirrored delta and theta components of the PSD. Delta-band synchronization often developed rapidly when animals paused briefly between runs, as well as appearing throughout longer 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 amongst theta-dominated modes during navigation. As such these modes of mPFC-HC circuit dynamics could play a fundamental role in coordinating encoding and retrieval mechanisms or decision-making processes at a timescale that segments event sequences within behavioral episodes.

Functionally distinct high and low theta oscillations in the human hippocampus

“…One potential explanation is that this signal, which we more often found in the anterior hippocampus, is related to the “Type 2” theta oscillations that had been characterized previously in rodents. Type 2 theta oscillations appear most strongly at ~4 Hz when rodents are stationary and are traditionally linked to anxiety (Kramis et al, 1975; Bland, 1986; Maren et al, 1994; Seidenbecher et al, 2003; Pape et al, 2005; but see Schultheiss et al, 2019). In contrast, current data from humans link oscillations in this low-theta band to memory processing (Lega et al, 2012; Lin et al, 2018; Miller et al, 2018).…”

Chronic Pb2+exposure causes theta-band hypersynchrony disrupting sensory motor gating and exacerbating absence seizures

“…All studies were carried out in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health under protocols approved by Florida International University Institutional Animal Care and Use Committee. Data from the four control rats in the electrophysiological experiments were previously analyzed to establish the relationships of hippocampal spectral modes to behaviors (Schultheiss et al, 2020). The present study focuses on the effects of Pb 2+ exposure and all analyses presented here are new.…”

“…Linking these levels requires animal models of Pb 2+ exposure allowing for invasive techniques that can establish a causal link between Pb 2+ exposure, specific neurobiological mechanisms, and behaviorally-relevant network consequences. Here, we performed chronic in vivo hippocampal recordings from a well-established rodent model of Pb 2+ exposure during open field behaviors (Schultheiss et al, 2020). This initial study of the rhythmic network effects of chronic Pb 2+ exposure focused on the hippocampus because chronic Pb 2+ -exposure causes reliable and severe deficits in hippocampal-dependent spatial learning (Kuhlmann et al, 1997; Jett et al, 199; Munoz et al, 1988) which can be ameliorated with environment enrichment (Cao et al, 2008; Guilarte et al, 2002), similar to other hippocampal insults.…”

Calretinin and calbindin architecture of the midline thalamus associated with prefrontal-hippocampal circuitry

“…Distinct CR + , CB + and CR + /CB + topographical zones in midline thalamus are likely associated with distinct rhythmicity like delta (e.g., Roy et al, 2017;Ferraris et al, 2018;Todorova and Zugaro, 2019;Schultheiss et al, 2020), theta (Hallock et al, 2016;Hasselmo et al, 2002;Jankowski et al, 2014;Lara-Vásquez et al, 2016;Roy et al, 2017;Vertes et al, 2004), or with sharp-wave ripples (Jadhav et al, 2012;Jadhav et al, 2016). Good support for this notion stems from the demonstration that CR + cells in midline thalamus exhibit distinct in vivo electrophysiological profiles (Lara-Vásquez et al, 2016).…”