Transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns

The inferior olive (IO) is a neural network belonging to the olivo-cerebellar system whose neurons are coupled with electrical synapses and display subthreshold oscillations and spiking activity. The IO is frequently proposed as the generator of timing signals to the cerebellum. Electrophysiological...

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Main Authors:	Latorre, Roberto, Aguirre, Carlos, Rabinovich, Mikhail I., Varona, Pablo
Format:	Online
Language:	English
Published:	Frontiers Media S.A. 2013
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3763220/

id	pubmed-3763220
recordtype	oai_dc
spelling	pubmed-37632202013-09-17 Transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns Latorre, Roberto Aguirre, Carlos Rabinovich, Mikhail I. Varona, Pablo Neuroscience The inferior olive (IO) is a neural network belonging to the olivo-cerebellar system whose neurons are coupled with electrical synapses and display subthreshold oscillations and spiking activity. The IO is frequently proposed as the generator of timing signals to the cerebellum. Electrophysiological and imaging recordings show that the IO network generates complex spatio-temporal patterns. The generation and modulation of coherent spiking activity in the IO is one key issue in cerebellar research. In this work, we build a large scale IO network model of electrically coupled conductance-based neurons to study the emerging spatio-temporal patterns of its transient neuronal activity. Our modeling reproduces and helps to understand important phenomena observed in IO in vitro and in vivo experiments, and draws new predictions regarding the computational properties of this network and the associated cerebellar circuits. The main factors studied governing the collective dynamics of the IO network were: the degree of electrical coupling, the extent of the electrotonic connections, the presence of stimuli or regions with different excitability levels and the modulatory effect of an inhibitory loop (IL). The spatio-temporal patterns were analyzed using a discrete wavelet transform to provide a quantitative characterization. Our results show that the electrotonic coupling produces quasi-synchronized subthreshold oscillations over a wide dynamical range. The synchronized oscillatory activity plays the role of a timer for a coordinated representation of spiking rhythms with different frequencies. The encoding and coexistence of several coordinated rhythms is related to the different clusterization and coherence of transient spatio-temporal patterns in the network, where the spiking activity is commensurate with the quasi-synchronized subthreshold oscillations. In the presence of stimuli, different rhythms are encoded in the spiking activity of the IO neurons that nevertheless remains constrained to a commensurate value of the subthreshold frequency. The stimuli induced spatio-temporal patterns can reverberate for long periods, which contributes to the computational properties of the IO. We also show that the presence of regions with different excitability levels creates sinks and sources of coordinated activity which shape the propagation of spike wave fronts. These results can be generalized beyond IO studies, as the control of wave pattern propagation is a highly relevant problem in the context of normal and pathological states in neural systems (e.g., related to tremor, migraine, epilepsy) where the study of the modulation of activity sinks and sources can have a potential large impact. Frontiers Media S.A. 2013-09-05 /pmc/articles/PMC3763220/ /pubmed/24046731 http://dx.doi.org/10.3389/fncir.2013.00138 Text en Copyright © 2013 Latorre, Aguirre, Rabinovich and Varona. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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	Latorre, Roberto Aguirre, Carlos Rabinovich, Mikhail I. Varona, Pablo
spellingShingle	Latorre, Roberto Aguirre, Carlos Rabinovich, Mikhail I. Varona, Pablo Transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns
author_facet	Latorre, Roberto Aguirre, Carlos Rabinovich, Mikhail I. Varona, Pablo
author_sort	Latorre, Roberto
title	Transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns
title_short	Transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns
title_full	Transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns
title_fullStr	Transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns
title_full_unstemmed	Transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns
title_sort	transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns
description	The inferior olive (IO) is a neural network belonging to the olivo-cerebellar system whose neurons are coupled with electrical synapses and display subthreshold oscillations and spiking activity. The IO is frequently proposed as the generator of timing signals to the cerebellum. Electrophysiological and imaging recordings show that the IO network generates complex spatio-temporal patterns. The generation and modulation of coherent spiking activity in the IO is one key issue in cerebellar research. In this work, we build a large scale IO network model of electrically coupled conductance-based neurons to study the emerging spatio-temporal patterns of its transient neuronal activity. Our modeling reproduces and helps to understand important phenomena observed in IO in vitro and in vivo experiments, and draws new predictions regarding the computational properties of this network and the associated cerebellar circuits. The main factors studied governing the collective dynamics of the IO network were: the degree of electrical coupling, the extent of the electrotonic connections, the presence of stimuli or regions with different excitability levels and the modulatory effect of an inhibitory loop (IL). The spatio-temporal patterns were analyzed using a discrete wavelet transform to provide a quantitative characterization. Our results show that the electrotonic coupling produces quasi-synchronized subthreshold oscillations over a wide dynamical range. The synchronized oscillatory activity plays the role of a timer for a coordinated representation of spiking rhythms with different frequencies. The encoding and coexistence of several coordinated rhythms is related to the different clusterization and coherence of transient spatio-temporal patterns in the network, where the spiking activity is commensurate with the quasi-synchronized subthreshold oscillations. In the presence of stimuli, different rhythms are encoded in the spiking activity of the IO neurons that nevertheless remains constrained to a commensurate value of the subthreshold frequency. The stimuli induced spatio-temporal patterns can reverberate for long periods, which contributes to the computational properties of the IO. We also show that the presence of regions with different excitability levels creates sinks and sources of coordinated activity which shape the propagation of spike wave fronts. These results can be generalized beyond IO studies, as the control of wave pattern propagation is a highly relevant problem in the context of normal and pathological states in neural systems (e.g., related to tremor, migraine, epilepsy) where the study of the modulation of activity sinks and sources can have a potential large impact.
publisher	Frontiers Media S.A.
publishDate	2013
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3763220/
_version_	1612008408136810496

Transient dynamics and rhythm coordination of inferior olive spatio-temporal patterns

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