Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat

By Anatol Bragin, G. Jandó, Zoltan Nadasdy, J. Hetke, K. Wise, György Buzsáki. 1995

The cellular generation and spatial distribution of gamma frequency (40– 100 Hz) activity was examined in the hippocampus of the awake rat. Field potentials and unit activity were recorded by multiple site silicon probes (5- and 16-site shanks) and wire electrode arrays. Gamma waves were highly coherent along the long axis of the dentate hilus, but average coherence decreased rapidly in the CA3 and CA1 directions. Analysis of short epochs revealed large fluctuations in coherence values between the dentate and CA1 gamma waves. Current source density analysis revealed large sinks and sources in the dentate gyrus with spatial distribution similar to the dipoles evoked by stimulation of the perforant path. The frequency changes of gamma and theta waves positively correlated (40–100 Hz and 5–10 Hz, respectively). Putative interneurons in the dentate gyrus discharged at gamma frequency and were phase-locked to the ascending part of the gamma waves recorded from the hilus. Following bilateral lesion of the entorhinal cortex the power and frequency of hilar gamma activity significantly decreased or disappeared. Instead, a large amplitude but slower gamma pattern (25–50 Hz) emerged in the CA3-CA1 network. We suggest that gamma oscillation emerges from an interaction between intrinsic oscillatory properties of interneurons and the network properties of the dentate gyrus. We also hypothesize that under physiological conditions the hilar gamma oscillation may be entrained by the entorhinal rhythm and that gamma oscillation in the CA3-CA1 circuitry is suppressed by either the hilar region or the entorhinal cortex.

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Citations in the corpus

Rapid Signaling at Inhibitory Synapses in a Dentate Gyrus Interneuron Network (2001, background): “Second, the requirement for a strong excitatory drive may explain the disappearance of gamma oscillations after lesioning of the entorhinal input (Bragin et al., 1995, their Fig.”
Neuronal gamma-band synchronization as a fundamental process in cortical computation. (2009, background): “It is clearly present in the hippocampus of awake behaving rats (Bragin et al. 1995, Csicsvari et al. 2003, Montgomery & Buzsáki 2007, Montgomery et al. 2008) and at different stages of the olfactory system of invertebrates (Wehr & Laurent 1996, Stopfer et al. 1997, Laurent 2002).”
A Proposed Function for Hippocampal Theta Rhythm: Separate Phases of Encoding and Retrieval Enhance Reversal of Prior Learning (2002, methodology): “Theta rhythm is associated with phasic changes in the magnitude of synaptic currents in different layers of thehippocampus,asshownbycurrentsourcedensityanalysisofhippocampal region CA1 (Buzsaki, Czopf, Kondakor, & Kellenyi, 1986; Brankack, Stewart, & Fox, 1993; Bragin et al., 1995 ).”
Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons (2000, background): “, Buzsaki et al., 1983; Bragin et al., 1995), the visual cortex of mammals, the olfactory cortex, the somatosensory cortex, and the thalamus (for a review, see Gray, 1994). Such oscillations have been also recorded in slices of the rat hippocampus (Whittington et al., 1995; Traub et al., 1996; Fisah”
Mechanisms of Gamma Oscillations (2012, background): “…their autocorrelograms and spectrograms at gamma frequency (Figure 3b), and the occurrence of their spikes follows those of the surrounding pyramidal neurons by a few milliseconds (Figure 3d, f ) (Bragin et al. 1995, Csicsvari et al. 2003, Mann et al. 2005, Hájos & Paulsen 2009), as in E-I models.”
Synaptic Properties of SOM- and CCK-Expressing Cells in Dentate Gyrus Interneuron Networks (2014, background): “High specificity in the dynamic properties in inhibitory signaling at HIPP–HIPP and HICAP–HICAP synapses During explorative behavior, the DG generates (4 –12 Hz)modulated (30 –100 Hz) activity patterns (Bragin et al., 1995; Leutgeb et al., 2007).”
CA3 Retrieves Coherent Representations from Degraded Input: Direct Evidence for CA3 Pattern Completion and Dentate Gyrus Pattern Separation (2014, background): “For tetrodes targeting DG, advancement was significantly reduced to 10–20 mm per day once gamma activity and dentate spikes in the LFP were detected (Bragin et al., 1995a, 1995b).”
What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. (2003, background): “…prominent gamma (40 – 80 Hz) rhythm during animal's free movement and rapid-eye movement (REM) sleep, and 200-Hz sharp-wave ripples during quiet sleep and immobility as measured by local field potential (LFP) (Bragin et al. 1995; Buzsaki et al. 1992; Csicsvari et al. 1999b; Siapas and Wilson 1998).”