Lateral and feedforward inhibition suppress asynchronous activity in a large, biophysically-detailed computational model of the striatal network

Striatal medium spiny neurons (MSNs) receive lateral inhibitory projections from other MSNs and feedforward inhibitory projections from fast-spiking, parvalbumin-containing striatal interneurons (FSIs). The functional roles of these connections are unknown, and difficult to study in an experimental...

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Main Authors: Jason T. Moyer, Benjamin L. Halterman, Leif H. Finkel, John A. Wolf
Format: Article
Language:English
Published: Frontiers Media S.A. 2014-11-01
Series:Frontiers in Computational Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fncom.2014.00152/full
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author Jason T. Moyer
Benjamin L. Halterman
Leif H. Finkel
John A. Wolf
author_facet Jason T. Moyer
Benjamin L. Halterman
Leif H. Finkel
John A. Wolf
author_sort Jason T. Moyer
collection DOAJ
description Striatal medium spiny neurons (MSNs) receive lateral inhibitory projections from other MSNs and feedforward inhibitory projections from fast-spiking, parvalbumin-containing striatal interneurons (FSIs). The functional roles of these connections are unknown, and difficult to study in an experimental preparation. We therefore investigated the functionality of both lateral (MSN-MSN) and feedforward (FSI-MSN) inhibition using a large-scale computational model of the striatal network. The model consists of 2744 MSNs comprised of 189 compartments each and 121 FSIs comprised of 148 compartments each, with dendrites explicitly represented and almost all known ionic currents included and strictly constrained by biological data as appropriate. Our analysis of the model indicates that both lateral inhibition and feedforward inhibition function at the population level to limit non-ensemble MSN spiking while preserving ensemble MSN spiking. Specifically, lateral inhibition enables large ensembles of MSNs firing synchronously to strongly suppress non-ensemble MSNs over a short time-scale (10-30 msec). Feedforward inhibition enables FSIs to strongly inhibit weakly activated, non-ensemble MSNs while moderately inhibiting activated ensemble MSNs. Importantly, FSIs appear to more effectively inhibit MSNs when FSIs fire asynchronously. Both types of inhibition would increase the signal-to-noise ratio of responding MSN ensembles and contribute to the formation and dissolution of MSN ensembles in the striatal network.
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spelling doaj.art-cc3202cce5f146d3bdd17855f08c3f0d2022-12-22T03:14:44ZengFrontiers Media S.A.Frontiers in Computational Neuroscience1662-51882014-11-01810.3389/fncom.2014.00152100037Lateral and feedforward inhibition suppress asynchronous activity in a large, biophysically-detailed computational model of the striatal networkJason T. Moyer0Benjamin L. Halterman1Leif H. Finkel2John A. Wolf3University of PennsylvaniaUniversity of PennsylvaniaUniversity of PennsylvaniaUniversity of PennsylvaniaStriatal medium spiny neurons (MSNs) receive lateral inhibitory projections from other MSNs and feedforward inhibitory projections from fast-spiking, parvalbumin-containing striatal interneurons (FSIs). The functional roles of these connections are unknown, and difficult to study in an experimental preparation. We therefore investigated the functionality of both lateral (MSN-MSN) and feedforward (FSI-MSN) inhibition using a large-scale computational model of the striatal network. The model consists of 2744 MSNs comprised of 189 compartments each and 121 FSIs comprised of 148 compartments each, with dendrites explicitly represented and almost all known ionic currents included and strictly constrained by biological data as appropriate. Our analysis of the model indicates that both lateral inhibition and feedforward inhibition function at the population level to limit non-ensemble MSN spiking while preserving ensemble MSN spiking. Specifically, lateral inhibition enables large ensembles of MSNs firing synchronously to strongly suppress non-ensemble MSNs over a short time-scale (10-30 msec). Feedforward inhibition enables FSIs to strongly inhibit weakly activated, non-ensemble MSNs while moderately inhibiting activated ensemble MSNs. Importantly, FSIs appear to more effectively inhibit MSNs when FSIs fire asynchronously. Both types of inhibition would increase the signal-to-noise ratio of responding MSN ensembles and contribute to the formation and dissolution of MSN ensembles in the striatal network.http://journal.frontiersin.org/Journal/10.3389/fncom.2014.00152/fullBasal GangliaParkinson DiseaseTourette Syndromecomputational modelinhibitionStriatum
spellingShingle Jason T. Moyer
Benjamin L. Halterman
Leif H. Finkel
John A. Wolf
Lateral and feedforward inhibition suppress asynchronous activity in a large, biophysically-detailed computational model of the striatal network
Frontiers in Computational Neuroscience
Basal Ganglia
Parkinson Disease
Tourette Syndrome
computational model
inhibition
Striatum
title Lateral and feedforward inhibition suppress asynchronous activity in a large, biophysically-detailed computational model of the striatal network
title_full Lateral and feedforward inhibition suppress asynchronous activity in a large, biophysically-detailed computational model of the striatal network
title_fullStr Lateral and feedforward inhibition suppress asynchronous activity in a large, biophysically-detailed computational model of the striatal network
title_full_unstemmed Lateral and feedforward inhibition suppress asynchronous activity in a large, biophysically-detailed computational model of the striatal network
title_short Lateral and feedforward inhibition suppress asynchronous activity in a large, biophysically-detailed computational model of the striatal network
title_sort lateral and feedforward inhibition suppress asynchronous activity in a large biophysically detailed computational model of the striatal network
topic Basal Ganglia
Parkinson Disease
Tourette Syndrome
computational model
inhibition
Striatum
url http://journal.frontiersin.org/Journal/10.3389/fncom.2014.00152/full
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