Theta-modulation drives the emergence of connectivity patterns underlying replay in a network model of place cells

Place cells of the rodent hippocampus fire action potentials when the animal traverses a particular spatial location in any environment. Therefore for any given trajectory one observes a repeatable sequence of place cell activations. When the animal is quiescent or sleeping, one can observe similar...

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Main Authors: Panagiota Theodoni, Bernat Rovira, Yingxue Wang, Alex Roxin
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/37388
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author Panagiota Theodoni
Bernat Rovira
Yingxue Wang
Alex Roxin
author_facet Panagiota Theodoni
Bernat Rovira
Yingxue Wang
Alex Roxin
author_sort Panagiota Theodoni
collection DOAJ
description Place cells of the rodent hippocampus fire action potentials when the animal traverses a particular spatial location in any environment. Therefore for any given trajectory one observes a repeatable sequence of place cell activations. When the animal is quiescent or sleeping, one can observe similar sequences of activation known as replay, which underlie the process of memory consolidation. However, it remains unclear how replay is generated. Here we show how a temporally asymmetric plasticity rule during spatial exploration gives rise to spontaneous replay in a model network by shaping the recurrent connectivity to reflect the topology of the learned environment. Crucially, the rate of this encoding is strongly modulated by ongoing rhythms. Oscillations in the theta range optimize learning by generating repeated pre-post pairings on a time-scale commensurate with the window for plasticity, while lower and higher frequencies generate learning rates which are lower by orders of magnitude.
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spelling doaj.art-b7bc61bbbd5b47e3affe0e6cf51301612022-12-22T03:24:33ZengeLife Sciences Publications LtdeLife2050-084X2018-10-01710.7554/eLife.37388Theta-modulation drives the emergence of connectivity patterns underlying replay in a network model of place cellsPanagiota Theodoni0Bernat Rovira1Yingxue Wang2Alex Roxin3https://orcid.org/0000-0003-1015-8138Centre de Recerca Matemàtica, Bellaterra, Spain; New York University Shanghai, Shanghai, China; NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai, Shanghai, ChinaCentre de Recerca Matemàtica, Bellaterra, Spain; Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, SpainMax Planck Florida Institute for Neuroscience, Jupiter, United StatesCentre de Recerca Matemàtica, Bellaterra, Spain; Barcelona Graduate School of Mathematics, Barcelona, SpainPlace cells of the rodent hippocampus fire action potentials when the animal traverses a particular spatial location in any environment. Therefore for any given trajectory one observes a repeatable sequence of place cell activations. When the animal is quiescent or sleeping, one can observe similar sequences of activation known as replay, which underlie the process of memory consolidation. However, it remains unclear how replay is generated. Here we show how a temporally asymmetric plasticity rule during spatial exploration gives rise to spontaneous replay in a model network by shaping the recurrent connectivity to reflect the topology of the learned environment. Crucially, the rate of this encoding is strongly modulated by ongoing rhythms. Oscillations in the theta range optimize learning by generating repeated pre-post pairings on a time-scale commensurate with the window for plasticity, while lower and higher frequencies generate learning rates which are lower by orders of magnitude.https://elifesciences.org/articles/37388hippocampusplasticityplace cellstheta oscillationreplaynetwork model
spellingShingle Panagiota Theodoni
Bernat Rovira
Yingxue Wang
Alex Roxin
Theta-modulation drives the emergence of connectivity patterns underlying replay in a network model of place cells
eLife
hippocampus
plasticity
place cells
theta oscillation
replay
network model
title Theta-modulation drives the emergence of connectivity patterns underlying replay in a network model of place cells
title_full Theta-modulation drives the emergence of connectivity patterns underlying replay in a network model of place cells
title_fullStr Theta-modulation drives the emergence of connectivity patterns underlying replay in a network model of place cells
title_full_unstemmed Theta-modulation drives the emergence of connectivity patterns underlying replay in a network model of place cells
title_short Theta-modulation drives the emergence of connectivity patterns underlying replay in a network model of place cells
title_sort theta modulation drives the emergence of connectivity patterns underlying replay in a network model of place cells
topic hippocampus
plasticity
place cells
theta oscillation
replay
network model
url https://elifesciences.org/articles/37388
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