Feedback Inhibition Enables Theta-Nested Gamma Oscillations and Grid Firing Fields

Hugh Pastoll,Lukas Solanka,Mark C.W Van Rossum,Matthew F Nolan

doi:10.1016/j.neuron.2012.11.032

Hugh Pastoll, Lukas Solanka + Show 2 more

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https://doi.org/10.1016/j.neuron.2012.11.032

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Journal: Neuron	Publication Date: Jan 1, 2013
Citations: 300	License type: elsevier-specific: oa user license

Affiliation: University of Edinburgh

Abstract

Cortical circuits are thought to multiplex firing rate codes with temporal codes that rely on oscillatory network activity, but the circuit mechanisms that combine these coding schemes are unclear. We establish with optogenetic activation of layer II of the medial entorhinal cortex that theta frequency drive to this circuit is sufficient to generate nested gamma frequency oscillations in synaptic activity. These nested gamma oscillations closely resemble activity during spatial exploration, are generated by local feedback inhibition without recurrent excitation, and have clock-like features suitable as reference signals for multiplexing temporal codes within rate-coded grid firing fields. In network models deduced from our data, feedback inhibition supports coexistence of theta-nested gamma oscillations with attractor states that generate grid firing fields. These results indicate that grid cells communicate primarily via inhibitory interneurons. This circuit mechanism enables multiplexing of oscillation-based temporal codes with rate-coded attractor states.

Highlights

Cortical neurons encode information through the rate and timing of their action potential output (Buzsaki and Draguhn, 2004; Fries, 2009; Huxter et al, 2003; O’Keefe and Recce, 1993)
Nested within the slower theta rhythm are network oscillations with frequency in the high gamma range (60–120 Hz) (Chrobak and Buzsaki, 1998; Colgin et al, 2009). These gamma frequency oscillations are believed to act as a reference signal to coordinate interactions between medial entorhinal cortex (MEC) neurons and their synaptic partners in the hippocampus (Buzsaki and Draguhn, 2004; Colgin et al, 2009), so that ensembles of MEC neurons with firing that is phase locked to nested gamma oscillations more effectively activate downstream neurons on which their synaptic output converges (Buzsaki and Wang, 2012; Fries, 2009)
We found that theta frequency (8 Hz) optical stimulation causes local field potential oscillations nested within each theta cycle (Figures 1A–1C)

Summary

Introduction

Cortical neurons encode information through the rate and timing of their action potential output (Buzsaki and Draguhn, 2004; Fries, 2009; Huxter et al, 2003; O’Keefe and Recce, 1993). Nested within the slower theta rhythm are network oscillations with frequency in the high gamma range (60–120 Hz) (Chrobak and Buzsaki, 1998; Colgin et al, 2009) These gamma frequency oscillations are believed to act as a reference signal to coordinate interactions between MEC neurons and their synaptic partners in the hippocampus (Buzsaki and Draguhn, 2004; Colgin et al, 2009), so that ensembles of MEC neurons with firing that is phase locked to nested gamma oscillations more effectively activate downstream neurons on which their synaptic output converges (Buzsaki and Wang, 2012; Fries, 2009). It is not clear if the same circuit mechanisms generate nested oscillatory activity and grid firing fields, or if instead either form of activity requires additional circuit elements

Results

Discussion

Conclusion