Identified Cellular Correlates of Neocortical Ripple and High-Gamma Oscillations during Spindles of Natural Sleep

Robert G Averkin,Viktor Szemenyei,Sándor Bordé,Gábor Tamás

doi:10.1016/j.neuron.2016.09.032

Robert G Averkin, Viktor Szemenyei + Show 2 more

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https://doi.org/10.1016/j.neuron.2016.09.032

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Journal: Neuron	Publication Date: Oct 13, 2016
Citations: 52	License type: cc-by

Affiliation: University of Szeged

Abstract

SummaryUltra-high-frequency network events in the hippocampus are instrumental in a dialogue with the neocortex during memory formation, but the existence of transient ∼200 Hz network events in the neocortex is not clear. Our recordings from neocortical layer II/III of freely behaving rats revealed field potential events at ripple and high-gamma frequencies repeatedly occurring at troughs of spindle oscillations during sleep. Juxtacellular recordings identified subpopulations of fast-spiking, parvalbumin-containing basket cells with epochs of firing at ripple (∼200 Hz) and high-gamma (∼120 Hz) frequencies detected during spindles and centered with millisecond precision at the trough of spindle waves in phase with field potential events but phase shifted relative to pyramidal cell firing. The results suggest that basket cell subpopulations are involved in spindle-nested, high-frequency network events that hypothetically provide repeatedly occurring neocortical temporal reference states potentially involved in mnemonic processes.

Highlights

Precise temporal structure is necessary for neuronal information transfer, and neuronal oscillations provide a temporal framework for this process (Klausberger and Somogyi, 2008; Salinas and Sejnowski, 2001; Singer and Gray, 1995)
Associated with alert states (Steriade, 2000), gamma, high-gamma, and ultra-high band (200–800 Hz) oscillations of local neocortical origin were observed in sleep (Hasenstaub et al, 2005; Kandel and Buzsaki, 1997); we asked whether spindle oscillations provide temporal reference for cellular and network correlates of neocortical high-frequency activity
High-Frequency Network Events Occur Repeatedly around Spindle Troughs Previous studies reported nesting of hippocampal ripples in parahippocampal/neocortical spindle activity in humans (Clemens et al, 2011; Staresina et al, 2015) and the presence of high-frequency oscillations near the trough of high-voltage spike-andwave spindles phase coupled to the firing of suspected interneurons in epileptic rat neocortex (Kandel and Buzsaki, 1997)

Summary

Introduction

Precise temporal structure is necessary for neuronal information transfer, and neuronal oscillations provide a temporal framework for this process (Klausberger and Somogyi, 2008; Salinas and Sejnowski, 2001; Singer and Gray, 1995). Sharp-wave-ripple-encoded, initial mnemonic representations in the hippocampus are followed by a consolidation stage performed in the neocortex (Born et al, 2006; Buzsaki, 1996; McClelland et al, 1995), but the existence of transient 200 Hz network events in the neocortex, potentially generated locally or by hippocampal inputs, is not clear. Associated with alert states (Steriade, 2000), gamma, high-gamma, and ultra-high band (200–800 Hz) oscillations of local neocortical origin were observed in sleep (Hasenstaub et al, 2005; Kandel and Buzsaki, 1997); we asked whether spindle oscillations provide temporal reference for cellular and network correlates of neocortical high-frequency activity

Results

Discussion

Conclusion