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Gap Junctions between Striatal Fast-Spiking Interneurons Regulate Spiking Activity and Synchronization as a Function of Cortical Activity
KTH, School of Computer Science and Communication (CSC), Computational Biology, CB.
KTH, School of Computer Science and Communication (CSC), Computational Biology, CB.ORCID iD: 0000-0002-0550-0739
2009 (English)In: Journal of Neuroscience, ISSN 0270-6474, E-ISSN 1529-2401, Vol. 29, no 16, 5276-5286 p.Article in journal (Refereed) Published
Abstract [en]

Striatal fast-spiking (FS) interneurons are interconnected by gap junctions into sparsely connected networks. As demonstrated for cortical FS interneurons, these gap junctions in the striatum may cause synchronized spiking, which would increase the influence that FS neurons have on spiking by the striatal medium spiny (MS) neurons. Dysfunction of the basal ganglia is characterized by changes in synchrony or periodicity, thus gap junctions between FS interneurons may modulate synchrony and thereby influence behavior such as reward learning and motor control. To explore the roles of gap junctions on activity and spike synchronization in a striatal FS population, we built a network model of FS interneurons. Each FS connects to 30-40% of its neighbors, as found experimentally, and each FS interneuron in the network is activated by simulated corticostriatal synaptic inputs. Our simulations show that the proportion of synchronous spikes in FS networks with gap junctions increases with increased conductance of the electrical synapse; however, the synchronization effects are moderate for experimentally estimated conductances. Instead, the main tendency is that the presence of gap junctions reduces the total number of spikes generated in response to synaptic inputs in the network. The reduction in spike firing is due to shunting through the gap junctions; which is minimized or absent when the neurons receive coincident inputs. Together these findings suggest that a population of electrically coupled FS interneurons may function collectively as input detectors that are especially sensitive to synchronized synaptic inputs received from the cortex.

Place, publisher, year, edition, pages
2009. Vol. 29, no 16, 5276-5286 p.
Keyword [en]
timing-dependent plasticity; electrical synapses; basal ganglia; gabaergic interneurons; spiny neurons; corticostriatal synapses; synaptic plasticity; projection neurons; in-vitro; states
National Category
Computer Science
Identifiers
URN: urn:nbn:se:kth:diva-14150DOI: 10.1523/JNEUROSCI.6031-08.2009ISI: 000265450300026Scopus ID: 2-s2.0-65549166921OAI: oai:DiVA.org:kth-14150DiVA: diva2:330829
Note
QC 20100720Available from: 2010-07-20 Created: 2010-07-20 Last updated: 2017-12-12Bibliographically approved
In thesis
1. Computer Modelling of Neuronal Interactions in the Striatum
Open this publication in new window or tab >>Computer Modelling of Neuronal Interactions in the Striatum
2009 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Large parts of the cortex and the thalamus project into the striatum,which serves as the input stage of the basal ganglia. Information isintegrated in the striatal neural network and then passed on, via themedium spiny (MS) projection neurons, to the output stages of thebasal ganglia. In addition to the MS neurons there are also severaltypes of interneurons in the striatum, such as the fast spiking (FS)interneurons. I focused my research on the FS neurons, which formstrong inhibitory synapses onto the MS neurons. These striatal FSneurons are sparsely connected by electrical synapses (gap junctions),which are commonly presumed to synchronise their activity.Computational modelling with the GENESIS simulator was used toinvestigate the effect of gap junctions on a network of synapticallydriven striatal FS neurons. The simulations predicted a reduction infiring frequency dependent on the correlation between synaptic inputsto the neighbouring neurons, but only a slight synchronisation. Thegap junction effects on modelled FS neurons showing sub-thresholdoscillations and stuttering behaviour confirm these results andfurther indicate that hyperpolarising inputs might regulate the onsetof stuttering.The interactions between MS and FS neurons were investigated byincluding a computer model of the MS neuron. The hypothesis was thatdistal GABAergic input would lower the amplitude of back propagatingaction potentials, thereby reducing the calcium influx in thedendrites. The model verified this and further predicted that proximalGABAergic input controls spike timing, but not the amplitude ofdendritic calcium influx after initiation.Connecting models of neurons written in different simulators intonetworks raised technical problems which were resolved by integratingthe simulators within the MUSIC framework. This thesis discusses theissues encountered by using this implementation and gives instructionsfor modifying MOOSE scripts to use MUSIC and provides guidelines forachieving compatibility between MUSIC and other simulators.This work sheds light on the interactions between striatal FS and MSneurons. The quantitative results presented could be used to developa large scale striatal network model in the future, which would beapplicable to both the healthy and pathological striatum.

Place, publisher, year, edition, pages
Stockholm: KTH, 2009. 79 p.
Series
Trita-CSC-A, ISSN 1653-5723 ; 2009:08
Keyword
striatum, fast spiking interneurons, medium spiny projection neurons, gap junctions, interoperability, MUSIC
National Category
Computer Science
Identifiers
urn:nbn:se:kth:diva-10523 (URN)978-91-7415-331-6 (ISBN)
Public defence
2009-06-11, Svedbergssalen (FD5), Roslagstullsbacken 21, Alba Nova, 09:00 (English)
Opponent
Supervisors
Note
QC 20100720Available from: 2009-06-03 Created: 2009-05-20 Last updated: 2010-07-20Bibliographically approved

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