Abstract
SummaryTheta oscillations reflect rhythmic inputs that continuously converge to the hippocampus during exploratory and memory-guided behavior. The theta-nested operations that organize hippocampal spiking could either occur regularly from one cycle to the next or be tuned on a cycle-by-cycle basis. To resolve this, we identified spectral components nested in individual theta cycles recorded from the mouse CA1 hippocampus. Our single-cycle profiling revealed theta spectral components associated with different firing modulations and distinguishable ensembles of principal cells. Moreover, novel co-firing patterns of principal cells in theta cycles nesting mid-gamma oscillations were the most strongly reactivated in subsequent offline sharp-wave/ripple events. Finally, theta-nested spectral components were differentially altered by behavioral stages of a memory task; the 80-Hz mid-gamma component was strengthened during learning, whereas the 22-Hz beta, 35-Hz slow gamma, and 54-Hz mid-gamma components increased during retrieval. We conclude that cycle-to-cycle variability of theta-nested spectral components allows parsing of theta oscillations into transient operating modes with complementary mnemonic roles.
Highlights
Neuronal activity in the hippocampal circuit is organized on multiple timescales by a collection of network oscillators (Buzsaki, 2010)
Profiling Individual Theta Cycles by Their Spectral Content We aimed to characterize the spectral signature of individual theta cycles observed in local field potentials (LFPs) of the CA1 pyramidal cell layer
Theta-Nested Spectral Components Are Associated with Different Firing Modulation of Principal Cells In line with the previous analysis (Figure 1), we found that the relationship between the strength of each theta-nested spectral components (tSCs) and theta phase was robust across the whole mouse dataset (Figures 2A and S3C)
Summary
Neuronal activity in the hippocampal circuit is organized on multiple timescales by a collection of network oscillators (Buzsaki, 2010). In the hippocampal CA1 area, this broad frequency range has been subdivided into slow ($30–50 Hz) and mid ($50–100 Hz) gamma oscillations, which present maximum amplitude at distinct theta phases (Belluscio et al, 2012; Colgin et al, 2009; Middleton and McHugh, 2016; Scheffer-Teixeira et al, 2012; Yamamoto et al, 2014) and emerge from separate locations along the somato-dendritic axis of CA1 principal cells (Lasztoczi and Klausberger, 2016; Schomburg et al, 2014), whereas fast ($100–140 Hz) gamma components originate from the pyramidal layer (Lasztoczi and Klausberger, 2016; Schomburg et al, 2014) These gamma band oscillations reflect the synchronous activity of distinct neuronal circuits (Bragin et al, 1995; Colgin et al, 2009; Csicsvari et al, 2003; Fernandez-Ruiz et al, 2017; Lasztoczi and Klausberger, 2014) and could correspond to different network states (Carr and Frank, 2012; Colgin, 2015b). We hypothesized that the cycleby-cycle variability of theta-nested oscillations reports flexible switching of the hippocampal network between different operating modes, such as memory encoding and retrieval
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