Intrinsic Cellular Properties and Connectivity Density Determine Variable Clustering Patterns in Randomly Connected Inhibitory Neural Networks

The plethora of inhibitory interneurons in the hippocampus and cortex play a pivotal role in generating rhythmic activity by clustering and synchronizing cell firing. Results of our simulations demonstrate that both the intrinsic cellular properties of neurons and the degree of network connectivity...

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Main Authors: Scott Rich, Victoria Booth, Michal Zochowski
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-10-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fncir.2016.00082/full
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author Scott Rich
Victoria Booth
Michal Zochowski
author_facet Scott Rich
Victoria Booth
Michal Zochowski
author_sort Scott Rich
collection DOAJ
description The plethora of inhibitory interneurons in the hippocampus and cortex play a pivotal role in generating rhythmic activity by clustering and synchronizing cell firing. Results of our simulations demonstrate that both the intrinsic cellular properties of neurons and the degree of network connectivity affect the characteristics of clustered dynamics exhibited in randomly connected, heterogeneous inhibitory networks. We quantify intrinsic cellular properties by the neuron's current-frequency relation (IF curve) and Phase Response Curve (PRC), a measure of how perturbations given at various phases of a neuron’s firing cycle affect subsequent spike timing. We analyze network bursting properties of networks of neurons with Type I or Type II properties in both excitability and PRC profile; Type I PRCs strictly show phase advances and IF curves that exhibit frequencies arbitrarily close to zero at firing threshold while Type II PRCs display both phase advances and delays and IF curves that have a non-zero frequency at threshold. Type II neurons whose properties arise with or without an M-type adaptation current are considered. We analyze network dynamics under different levels of cellular heterogeneity and as intrinsic cellular firing frequency and the time scale of decay of synaptic inhibition are varied. Many of the dynamics exhibited by these networks diverge from the predictions of the interneuron network gamma (ING) mechanism, as well as from results in all-to-all connected networks. Our results show that randomly connected networks of Type I neurons synchronize into a single cluster of active neurons while networks of Type II neurons organize into two mutually exclusive clusters segregated by the cells' intrinsic firing frequencies. Networks of Type II neurons containing the adaptation current behave similarly to networks of either Type I or Type II neurons depending on network parameters; however, the adaptation current creates differences in the cluster dynamics compared to those in networks of Type I or Type II neurons. To understand these results, we compute neuronal PRCs calculated with a perturbation matching the profile of the synaptic current in our networks. Differences in profiles of these PRCs across the different neuron types reveal mechanisms underlying the divergent network dynamics.
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spelling doaj.art-8871e439064e42b98b9832061a2cdab52022-12-21T20:02:23ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102016-10-011010.3389/fncir.2016.00082216629Intrinsic Cellular Properties and Connectivity Density Determine Variable Clustering Patterns in Randomly Connected Inhibitory Neural NetworksScott Rich0Victoria Booth1Michal Zochowski2University of MichiganUniversity of MichiganUniversity of MichiganThe plethora of inhibitory interneurons in the hippocampus and cortex play a pivotal role in generating rhythmic activity by clustering and synchronizing cell firing. Results of our simulations demonstrate that both the intrinsic cellular properties of neurons and the degree of network connectivity affect the characteristics of clustered dynamics exhibited in randomly connected, heterogeneous inhibitory networks. We quantify intrinsic cellular properties by the neuron's current-frequency relation (IF curve) and Phase Response Curve (PRC), a measure of how perturbations given at various phases of a neuron’s firing cycle affect subsequent spike timing. We analyze network bursting properties of networks of neurons with Type I or Type II properties in both excitability and PRC profile; Type I PRCs strictly show phase advances and IF curves that exhibit frequencies arbitrarily close to zero at firing threshold while Type II PRCs display both phase advances and delays and IF curves that have a non-zero frequency at threshold. Type II neurons whose properties arise with or without an M-type adaptation current are considered. We analyze network dynamics under different levels of cellular heterogeneity and as intrinsic cellular firing frequency and the time scale of decay of synaptic inhibition are varied. Many of the dynamics exhibited by these networks diverge from the predictions of the interneuron network gamma (ING) mechanism, as well as from results in all-to-all connected networks. Our results show that randomly connected networks of Type I neurons synchronize into a single cluster of active neurons while networks of Type II neurons organize into two mutually exclusive clusters segregated by the cells' intrinsic firing frequencies. Networks of Type II neurons containing the adaptation current behave similarly to networks of either Type I or Type II neurons depending on network parameters; however, the adaptation current creates differences in the cluster dynamics compared to those in networks of Type I or Type II neurons. To understand these results, we compute neuronal PRCs calculated with a perturbation matching the profile of the synaptic current in our networks. Differences in profiles of these PRCs across the different neuron types reveal mechanisms underlying the divergent network dynamics.http://journal.frontiersin.org/Journal/10.3389/fncir.2016.00082/fullInterneuronscomputational modelsynchronyclusteringphase response curvespike-frequency adaptation
spellingShingle Scott Rich
Victoria Booth
Michal Zochowski
Intrinsic Cellular Properties and Connectivity Density Determine Variable Clustering Patterns in Randomly Connected Inhibitory Neural Networks
Frontiers in Neural Circuits
Interneurons
computational model
synchrony
clustering
phase response curve
spike-frequency adaptation
title Intrinsic Cellular Properties and Connectivity Density Determine Variable Clustering Patterns in Randomly Connected Inhibitory Neural Networks
title_full Intrinsic Cellular Properties and Connectivity Density Determine Variable Clustering Patterns in Randomly Connected Inhibitory Neural Networks
title_fullStr Intrinsic Cellular Properties and Connectivity Density Determine Variable Clustering Patterns in Randomly Connected Inhibitory Neural Networks
title_full_unstemmed Intrinsic Cellular Properties and Connectivity Density Determine Variable Clustering Patterns in Randomly Connected Inhibitory Neural Networks
title_short Intrinsic Cellular Properties and Connectivity Density Determine Variable Clustering Patterns in Randomly Connected Inhibitory Neural Networks
title_sort intrinsic cellular properties and connectivity density determine variable clustering patterns in randomly connected inhibitory neural networks
topic Interneurons
computational model
synchrony
clustering
phase response curve
spike-frequency adaptation
url http://journal.frontiersin.org/Journal/10.3389/fncir.2016.00082/full
work_keys_str_mv AT scottrich intrinsiccellularpropertiesandconnectivitydensitydeterminevariableclusteringpatternsinrandomlyconnectedinhibitoryneuralnetworks
AT victoriabooth intrinsiccellularpropertiesandconnectivitydensitydeterminevariableclusteringpatternsinrandomlyconnectedinhibitoryneuralnetworks
AT michalzochowski intrinsiccellularpropertiesandconnectivitydensitydeterminevariableclusteringpatternsinrandomlyconnectedinhibitoryneuralnetworks