Impact of Adaptation Currents on Synchronization of Coupled Exponential Integrate-and-Fire Neurons

The ability of spiking neurons to synchronize their activity in a network depends on the response behavior of these neurons as quantified by the phase response curve (PRC) and on coupling properties. The PRC characterizes the effects of transient inputs on spike timing and can be measured experiment...

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Main Authors: Ladenbauer, Josef, Augustin, Moritz, Shiau, LieJune, Obermayer, Klaus
Format: Online
Language:English
Published: Public Library of Science 2012
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3325187/
id pubmed-3325187
recordtype oai_dc
spelling pubmed-33251872012-04-17 Impact of Adaptation Currents on Synchronization of Coupled Exponential Integrate-and-Fire Neurons Ladenbauer, Josef Augustin, Moritz Shiau, LieJune Obermayer, Klaus Research Article The ability of spiking neurons to synchronize their activity in a network depends on the response behavior of these neurons as quantified by the phase response curve (PRC) and on coupling properties. The PRC characterizes the effects of transient inputs on spike timing and can be measured experimentally. Here we use the adaptive exponential integrate-and-fire (aEIF) neuron model to determine how subthreshold and spike-triggered slow adaptation currents shape the PRC. Based on that, we predict how synchrony and phase locked states of coupled neurons change in presence of synaptic delays and unequal coupling strengths. We find that increased subthreshold adaptation currents cause a transition of the PRC from only phase advances to phase advances and delays in response to excitatory perturbations. Increased spike-triggered adaptation currents on the other hand predominantly skew the PRC to the right. Both adaptation induced changes of the PRC are modulated by spike frequency, being more prominent at lower frequencies. Applying phase reduction theory, we show that subthreshold adaptation stabilizes synchrony for pairs of coupled excitatory neurons, while spike-triggered adaptation causes locking with a small phase difference, as long as synaptic heterogeneities are negligible. For inhibitory pairs synchrony is stable and robust against conduction delays, and adaptation can mediate bistability of in-phase and anti-phase locking. We further demonstrate that stable synchrony and bistable in/anti-phase locking of pairs carry over to synchronization and clustering of larger networks. The effects of adaptation in aEIF neurons on PRCs and network dynamics qualitatively reflect those of biophysical adaptation currents in detailed Hodgkin-Huxley-based neurons, which underscores the utility of the aEIF model for investigating the dynamical behavior of networks. Our results suggest neuronal spike frequency adaptation as a mechanism synchronizing low frequency oscillations in local excitatory networks, but indicate that inhibition rather than excitation generates coherent rhythms at higher frequencies. Public Library of Science 2012-04-12 /pmc/articles/PMC3325187/ /pubmed/22511861 http://dx.doi.org/10.1371/journal.pcbi.1002478 Text en Ladenbauer et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Ladenbauer, Josef
Augustin, Moritz
Shiau, LieJune
Obermayer, Klaus
spellingShingle Ladenbauer, Josef
Augustin, Moritz
Shiau, LieJune
Obermayer, Klaus
Impact of Adaptation Currents on Synchronization of Coupled Exponential Integrate-and-Fire Neurons
author_facet Ladenbauer, Josef
Augustin, Moritz
Shiau, LieJune
Obermayer, Klaus
author_sort Ladenbauer, Josef
title Impact of Adaptation Currents on Synchronization of Coupled Exponential Integrate-and-Fire Neurons
title_short Impact of Adaptation Currents on Synchronization of Coupled Exponential Integrate-and-Fire Neurons
title_full Impact of Adaptation Currents on Synchronization of Coupled Exponential Integrate-and-Fire Neurons
title_fullStr Impact of Adaptation Currents on Synchronization of Coupled Exponential Integrate-and-Fire Neurons
title_full_unstemmed Impact of Adaptation Currents on Synchronization of Coupled Exponential Integrate-and-Fire Neurons
title_sort impact of adaptation currents on synchronization of coupled exponential integrate-and-fire neurons
description The ability of spiking neurons to synchronize their activity in a network depends on the response behavior of these neurons as quantified by the phase response curve (PRC) and on coupling properties. The PRC characterizes the effects of transient inputs on spike timing and can be measured experimentally. Here we use the adaptive exponential integrate-and-fire (aEIF) neuron model to determine how subthreshold and spike-triggered slow adaptation currents shape the PRC. Based on that, we predict how synchrony and phase locked states of coupled neurons change in presence of synaptic delays and unequal coupling strengths. We find that increased subthreshold adaptation currents cause a transition of the PRC from only phase advances to phase advances and delays in response to excitatory perturbations. Increased spike-triggered adaptation currents on the other hand predominantly skew the PRC to the right. Both adaptation induced changes of the PRC are modulated by spike frequency, being more prominent at lower frequencies. Applying phase reduction theory, we show that subthreshold adaptation stabilizes synchrony for pairs of coupled excitatory neurons, while spike-triggered adaptation causes locking with a small phase difference, as long as synaptic heterogeneities are negligible. For inhibitory pairs synchrony is stable and robust against conduction delays, and adaptation can mediate bistability of in-phase and anti-phase locking. We further demonstrate that stable synchrony and bistable in/anti-phase locking of pairs carry over to synchronization and clustering of larger networks. The effects of adaptation in aEIF neurons on PRCs and network dynamics qualitatively reflect those of biophysical adaptation currents in detailed Hodgkin-Huxley-based neurons, which underscores the utility of the aEIF model for investigating the dynamical behavior of networks. Our results suggest neuronal spike frequency adaptation as a mechanism synchronizing low frequency oscillations in local excitatory networks, but indicate that inhibition rather than excitation generates coherent rhythms at higher frequencies.
publisher Public Library of Science
publishDate 2012
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3325187/
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