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 net...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2014-02-01
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| Series: | Frontiers in Neural Circuits |
| Subjects: | |
| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fncir.2014.00010/full |
| _version_ | 1818473795391848448 |
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| author | Pedro J Goncalves Aristides B Arrenberg Bastian eHablitzel Herwig eBaier Christian K Machens |
| author_facet | Pedro J Goncalves Aristides B Arrenberg Bastian eHablitzel Herwig eBaier Christian K Machens |
| author_sort | Pedro J Goncalves |
| collection | DOAJ |
| 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 towards 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. |
| first_indexed | 2024-04-14T04:27:11Z |
| format | Article |
| id | doaj.art-3ccc6ae5b7a54beda897cfca905b2684 |
| institution | Directory Open Access Journal |
| issn | 1662-5110 |
| language | English |
| last_indexed | 2024-04-14T04:27:11Z |
| publishDate | 2014-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj.art-3ccc6ae5b7a54beda897cfca905b26842022-12-22T02:12:13ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102014-02-01810.3389/fncir.2014.0001047745Optogenetic perturbations reveal the dynamics of an oculomotor integratorPedro J Goncalves0Aristides B Arrenberg1Bastian eHablitzel2Herwig eBaier3Christian K Machens4University College LondonUniversity of FreiburgUniversity of FreiburgMax Planck Institute of NeurobiologyChampalimaud FoundationMany 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 towards 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.http://journal.frontiersin.org/Journal/10.3389/fncir.2014.00010/fullZebrafishnetwork dynamicsoptogeneticsModeloculomotor systemneural integrator |
| spellingShingle | Pedro J Goncalves Aristides B Arrenberg Bastian eHablitzel Herwig eBaier Christian K Machens Optogenetic perturbations reveal the dynamics of an oculomotor integrator Frontiers in Neural Circuits Zebrafish network dynamics optogenetics Model oculomotor system neural integrator |
| title | 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_short | Optogenetic perturbations reveal the dynamics of an oculomotor integrator |
| title_sort | optogenetic perturbations reveal the dynamics of an oculomotor integrator |
| topic | Zebrafish network dynamics optogenetics Model oculomotor system neural integrator |
| url | http://journal.frontiersin.org/Journal/10.3389/fncir.2014.00010/full |
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