Optogenetic perturbations reveal the dynamics of an oculomotor integrator

Many neural systems can store short-term information in persistently firing neurons. Such persistent activity is believed to be maintained by recurrent feedback among neurons. This hypothesis has been fleshed out in detail for the oculomotor integrator (OI) for which the so-called “line attractor” n...

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Main Authors:	Gonçalves, Pedro J., Arrenberg, Aristides B., Hablitzel, Bastian, Baier, Herwig, Machens, Christian K.
Format:	Online
Language:	English
Published:	Frontiers Media S.A. 2014
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3937552/

id	pubmed-3937552
recordtype	oai_dc
spelling	pubmed-39375522014-03-10 Optogenetic perturbations reveal the dynamics of an oculomotor integrator Gonçalves, Pedro J. Arrenberg, Aristides B. Hablitzel, Bastian Baier, Herwig Machens, Christian K. Neuroscience Many neural systems can store short-term information in persistently firing neurons. Such persistent activity is believed to be maintained by recurrent feedback among neurons. This hypothesis has been fleshed out in detail for the oculomotor integrator (OI) for which the so-called “line attractor” network model can explain a large set of observations. Here we show that there is a plethora of such models, distinguished by the relative strength of recurrent excitation and inhibition. In each model, the firing rates of the neurons relax toward the persistent activity states. The dynamics of relaxation can be quite different, however, and depend on the levels of recurrent excitation and inhibition. To identify the correct model, we directly measure these relaxation dynamics by performing optogenetic perturbations in the OI of zebrafish expressing halorhodopsin or channelrhodopsin. We show that instantaneous, inhibitory stimulations of the OI lead to persistent, centripetal eye position changes ipsilateral to the stimulation. Excitatory stimulations similarly cause centripetal eye position changes, yet only contralateral to the stimulation. These results show that the dynamics of the OI are organized around a central attractor state—the null position of the eyes—which stabilizes the system against random perturbations. Our results pose new constraints on the circuit connectivity of the system and provide new insights into the mechanisms underlying persistent activity. Frontiers Media S.A. 2014-02-28 /pmc/articles/PMC3937552/ /pubmed/24616666 http://dx.doi.org/10.3389/fncir.2014.00010 Text en Copyright © 2014 Gonçalves, Arrenberg, Hablitzel, Baier and Machens. 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	Gonçalves, Pedro J. Arrenberg, Aristides B. Hablitzel, Bastian Baier, Herwig Machens, Christian K.
spellingShingle	Gonçalves, Pedro J. Arrenberg, Aristides B. Hablitzel, Bastian Baier, Herwig Machens, Christian K. Optogenetic perturbations reveal the dynamics of an oculomotor integrator
author_facet	Gonçalves, Pedro J. Arrenberg, Aristides B. Hablitzel, Bastian Baier, Herwig Machens, Christian K.
author_sort	Gonçalves, Pedro J.
title	Optogenetic perturbations reveal the dynamics of an oculomotor integrator
title_short	Optogenetic perturbations reveal the dynamics of an oculomotor integrator
title_full	Optogenetic perturbations reveal the dynamics of an oculomotor integrator
title_fullStr	Optogenetic perturbations reveal the dynamics of an oculomotor integrator
title_full_unstemmed	Optogenetic perturbations reveal the dynamics of an oculomotor integrator
title_sort	optogenetic perturbations reveal the dynamics of an oculomotor integrator
description	Many neural systems can store short-term information in persistently firing neurons. Such persistent activity is believed to be maintained by recurrent feedback among neurons. This hypothesis has been fleshed out in detail for the oculomotor integrator (OI) for which the so-called “line attractor” network model can explain a large set of observations. Here we show that there is a plethora of such models, distinguished by the relative strength of recurrent excitation and inhibition. In each model, the firing rates of the neurons relax toward the persistent activity states. The dynamics of relaxation can be quite different, however, and depend on the levels of recurrent excitation and inhibition. To identify the correct model, we directly measure these relaxation dynamics by performing optogenetic perturbations in the OI of zebrafish expressing halorhodopsin or channelrhodopsin. We show that instantaneous, inhibitory stimulations of the OI lead to persistent, centripetal eye position changes ipsilateral to the stimulation. Excitatory stimulations similarly cause centripetal eye position changes, yet only contralateral to the stimulation. These results show that the dynamics of the OI are organized around a central attractor state—the null position of the eyes—which stabilizes the system against random perturbations. Our results pose new constraints on the circuit connectivity of the system and provide new insights into the mechanisms underlying persistent activity.
publisher	Frontiers Media S.A.
publishDate	2014
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3937552/
_version_	1612062896883236864

Optogenetic perturbations reveal the dynamics of an oculomotor integrator

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