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Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation

Reciprocal inhibition is a building block in many sensory and motor circuits. We studied the features that underly robustness in reciprocally inhibitory two neuron circuits. We used the dynamic clamp to create reciprocally inhibitory circuits from pharmacologically isolated neurons of the crab stoma...

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Autores principales: Morozova, Ekaterina, Newstein, Peter, Marder, Eve
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8884723/
https://www.ncbi.nlm.nih.gov/pubmed/35103594
http://dx.doi.org/10.7554/eLife.74363
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author Morozova, Ekaterina
Newstein, Peter
Marder, Eve
author_facet Morozova, Ekaterina
Newstein, Peter
Marder, Eve
author_sort Morozova, Ekaterina
collection PubMed
description Reciprocal inhibition is a building block in many sensory and motor circuits. We studied the features that underly robustness in reciprocally inhibitory two neuron circuits. We used the dynamic clamp to create reciprocally inhibitory circuits from pharmacologically isolated neurons of the crab stomatogastric ganglion by injecting artificial graded synaptic (I(Syn)) and hyperpolarization-activated inward (I(H)) currents. There is a continuum of mechanisms in circuits that generate antiphase oscillations, with ‘release’ and ‘escape’ mechanisms at the extremes, and mixed mode oscillations between these extremes. In release, the active neuron primarily controls the off/on transitions. In escape, the inhibited neuron controls the transitions. We characterized the robustness of escape and release circuits to alterations in circuit parameters, temperature, and neuromodulation. We found that escape circuits rely on tight correlations between synaptic and H conductances to generate bursting but are resilient to temperature increase. Release circuits are robust to variations in synaptic and H conductances but fragile to temperature increase. The modulatory current (I(MI)) restores oscillations in release circuits but has little effect in escape circuits. Perturbations can alter the balance of escape and release mechanisms and can create mixed mode oscillations. We conclude that the same perturbation can have dramatically different effects depending on the circuits’ mechanism of operation that may not be observable from basal circuit activity.
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spelling pubmed-88847232022-03-01 Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation Morozova, Ekaterina Newstein, Peter Marder, Eve eLife Neuroscience Reciprocal inhibition is a building block in many sensory and motor circuits. We studied the features that underly robustness in reciprocally inhibitory two neuron circuits. We used the dynamic clamp to create reciprocally inhibitory circuits from pharmacologically isolated neurons of the crab stomatogastric ganglion by injecting artificial graded synaptic (I(Syn)) and hyperpolarization-activated inward (I(H)) currents. There is a continuum of mechanisms in circuits that generate antiphase oscillations, with ‘release’ and ‘escape’ mechanisms at the extremes, and mixed mode oscillations between these extremes. In release, the active neuron primarily controls the off/on transitions. In escape, the inhibited neuron controls the transitions. We characterized the robustness of escape and release circuits to alterations in circuit parameters, temperature, and neuromodulation. We found that escape circuits rely on tight correlations between synaptic and H conductances to generate bursting but are resilient to temperature increase. Release circuits are robust to variations in synaptic and H conductances but fragile to temperature increase. The modulatory current (I(MI)) restores oscillations in release circuits but has little effect in escape circuits. Perturbations can alter the balance of escape and release mechanisms and can create mixed mode oscillations. We conclude that the same perturbation can have dramatically different effects depending on the circuits’ mechanism of operation that may not be observable from basal circuit activity. eLife Sciences Publications, Ltd 2022-02-01 /pmc/articles/PMC8884723/ /pubmed/35103594 http://dx.doi.org/10.7554/eLife.74363 Text en © 2022, Morozova et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Morozova, Ekaterina
Newstein, Peter
Marder, Eve
Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation
title Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation
title_full Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation
title_fullStr Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation
title_full_unstemmed Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation
title_short Reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation
title_sort reciprocally inhibitory circuits operating with distinct mechanisms are differently robust to perturbation and modulation
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8884723/
https://www.ncbi.nlm.nih.gov/pubmed/35103594
http://dx.doi.org/10.7554/eLife.74363
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AT mardereve reciprocallyinhibitorycircuitsoperatingwithdistinctmechanismsaredifferentlyrobusttoperturbationandmodulation