Abstract
Multiple components of “γ-oscillations” between 30–170 Hz in the CA1 region of the hippocampus have been described, based on their coherence with oscillations in other brain regions and on their cross-frequency coupling with local θ-oscillations. However, it remains unclear whether the different sub-bands are generated by a single broadband oscillator coupled to multiple external inputs, or by separate oscillators that incorporate distinct circuit elements. To distinguish between these possibilities, we used high-density linear array recording electrodes in awake behaving mice to examine the spatiotemporal characteristics of γ-oscillations and their responses to midazolam and atropine. We characterized oscillations using current source density (CSD) analysis, and measured θ-γ phase-amplitude coupling by cross frequency coupling (CFC) analysis. Prominent peaks were present in the CSD signal in the mid- and distal apical dendritic layers at all frequencies, and at stratum pyramidale for γslow (30–45 Hz) and γmid (50–90 Hz), but not γfast (90–170 Hz) oscillations. Differences in the strength and timing of θ-γslow and θ-γmid cross frequency coupling, and a lack of coupling at the soma and mid-apical region for γfast oscillations, indicated that separate circuit components generate the three sub-bands. Midazolam altered CSD amplitudes and cross-frequency coupling in a lamina- and frequency specific manner, providing further evidence for separate generator circuits. Atropine altered CSD amplitudes and θ-γ CFC uniformly at all locations. Simulations using a detailed compartmental model were consistent with γslow and γmid oscillations driven primarily by inputs at the mid-apical dendrites, and γfast at the distal apical dendrite. Our results indicate that multiple distinct local circuits generate γ-oscillations in the CA1 region of the hippocampus, and provide detailed information about their spatiotemporal characteristics.
Highlights
Oscillations in the brain span a wide range of frequencies and play a variety of roles in different brain structures
We examined the spatial pattern of the current sinks and sources that produce each of the three higher frequency bands using current source density (CSD) analysis
Compared to the D-ADpole and M-ADpole, which were consistently present in all recordings in all animals, the Spole showed substantial variability between animals; it was not discernible in the γslow band in two mice, or in the γmid band in four mice, and it was completely absent in the γfast oscillations in all mice
Summary
Oscillations in the brain span a wide range of frequencies and play a variety of roles in different brain structures. Unlike the θ-oscillation, which is sufficiently large, widespread, and regular that it creates a distinct peak in the power spectrum, γ-oscillations occur over a relatively broad range of frequencies, and there are no distinct peaks within this range. Based upon their coherence with γ-oscillations in other structures, γ-oscillations in the CA1 region have been separated into slow (25–50 Hz) and fast (50–140 Hz) γ-oscillations, driven by inputs from the CA3 region and entorhinal cortex (ECtx) respectively (Bragin et al, 1995; Charpak et al, 1995; Middleton et al, 2008; Colgin et al, 2009). Additional studies of cross-frequency coupling (CFC) between θ- and γ-oscillations in the CA1 region have further subdivided the faster component into mid (50–90 Hz) and high frequency oscillations (90–170 Hz) (Belluscio et al, 2012; Buzsáki and Wang, 2012; Tort et al, 2012)
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