Feedback inhibition enables theta-nested gamma oscillations and grid firing fields

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 freque...

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Main Authors: Pastoll, Hugh, Solanka, Lukas, van Rossum, Mark C.W., Nolan, Matthew F.
Format: Article
Published: Elsevier 2013
Online Access:https://eprints.nottingham.ac.uk/49638/
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author Pastoll, Hugh
Solanka, Lukas
van Rossum, Mark C.W.
Nolan, Matthew F.
author_facet Pastoll, Hugh
Solanka, Lukas
van Rossum, Mark C.W.
Nolan, Matthew F.
author_sort Pastoll, Hugh
building Nottingham Research Data Repository
collection Online Access
description 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.
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spelling nottingham-496382020-05-04T16:35:35Z https://eprints.nottingham.ac.uk/49638/ Feedback inhibition enables theta-nested gamma oscillations and grid firing fields Pastoll, Hugh Solanka, Lukas van Rossum, Mark C.W. Nolan, Matthew F. 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. Elsevier 2013-01-09 Article PeerReviewed Pastoll, Hugh, Solanka, Lukas, van Rossum, Mark C.W. and Nolan, Matthew F. (2013) Feedback inhibition enables theta-nested gamma oscillations and grid firing fields. Neuron, 77 (1). pp. 141-54. ISSN 1097-4199 https://www.sciencedirect.com/science/article/pii/S0896627312011191 doi:10.1016/j.neuron.2012.11.032 doi:10.1016/j.neuron.2012.11.032
spellingShingle Pastoll, Hugh
Solanka, Lukas
van Rossum, Mark C.W.
Nolan, Matthew F.
Feedback inhibition enables theta-nested gamma oscillations and grid firing fields
title Feedback inhibition enables theta-nested gamma oscillations and grid firing fields
title_full Feedback inhibition enables theta-nested gamma oscillations and grid firing fields
title_fullStr Feedback inhibition enables theta-nested gamma oscillations and grid firing fields
title_full_unstemmed Feedback inhibition enables theta-nested gamma oscillations and grid firing fields
title_short Feedback inhibition enables theta-nested gamma oscillations and grid firing fields
title_sort feedback inhibition enables theta-nested gamma oscillations and grid firing fields
url https://eprints.nottingham.ac.uk/49638/
https://eprints.nottingham.ac.uk/49638/
https://eprints.nottingham.ac.uk/49638/