Electrical Synapses Enhance and Accelerate Interneuron Recruitment in Response to Coincident and Sequential Excitation
Electrical synapses are ubiquitous in interneuron networks. They form intercellular pathways, allowing electrical currents to leak between coupled interneurons. I explored the impact of electrical coupling on the integration of excitatory signals and on the coincidence detection abilities of electri...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-06-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fncel.2018.00156/full |
| _version_ | 1811194947539304448 |
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| author | Pepe Alcami Pepe Alcami Pepe Alcami Pepe Alcami |
| author_facet | Pepe Alcami Pepe Alcami Pepe Alcami Pepe Alcami |
| author_sort | Pepe Alcami |
| collection | DOAJ |
| description | Electrical synapses are ubiquitous in interneuron networks. They form intercellular pathways, allowing electrical currents to leak between coupled interneurons. I explored the impact of electrical coupling on the integration of excitatory signals and on the coincidence detection abilities of electrically-coupled cerebellar basket cells (BCs). In order to do so, I quantified the influence of electrical coupling on the rate, the probability and the latency at which BCs generate action potentials when stimulated. The long-lasting simultaneous suprathreshold depolarization of a coupled cell evoked an increase in firing rate and a shortening of action potential latency in a reference basket cell, compared to its depolarization alone. Likewise, the action potential probability of coupled cells was strongly increased when they were simultaneously stimulated with trains of short-duration near-threshold current pulses (mimicking the activation of presynaptic granule cells) at 10 Hz, and to a lesser extent at 50 Hz, an effect that was absent in non-coupled cells. Moreover, action potential probability was increased and action potential latency was shortened in response to synaptic stimulations in mice lacking the protein that forms gap junctions between BCs, connexin36, relative to wild-type (WT) controls. These results suggest that electrical synapses between BCs decrease the probability and increase the latency of stimulus-triggered action potentials, both effects being reverted upon simultaneous excitation of coupled cells. Interestingly, varying the delay at which coupled cells are stimulated revealed that the probability and the speed of action potential generation are facilitated maximally when a basket cell is stimulated shortly after a coupled cell. These findings suggest that electrically-coupled interneurons behave as coincidence and sequence detectors that dynamically regulate the latency and the strength of inhibition onto postsynaptic targets depending on the degree of input synchrony in the coupled interneuron network. |
| first_indexed | 2024-04-12T00:34:48Z |
| format | Article |
| id | doaj.art-f96ff7770f604248b47d0fcdd9119d38 |
| institution | Directory Open Access Journal |
| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-04-12T00:34:48Z |
| publishDate | 2018-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-f96ff7770f604248b47d0fcdd9119d382022-12-22T03:55:11ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022018-06-011210.3389/fncel.2018.00156204759Electrical Synapses Enhance and Accelerate Interneuron Recruitment in Response to Coincident and Sequential ExcitationPepe Alcami0Pepe Alcami1Pepe Alcami2Pepe Alcami3Laboratoire de Physiologie Cérébrale, Unité Mixte de Recherche UMR8118, Université Paris Descartes and Centre National de la Recherche Scientifique, Paris, FranceLaboratory of Cellular and Systemic Neurophysiology, Institute for Physiology I, Albert-Ludwigs University Freiburg, Freiburg, GermanyGrass Laboratory, Marine Biological Laboratory, Woods Hole, MA, United StatesDepartment of Behavioural Neurobiology, Max Planck Institute for Ornithology, Seewiesen, GermanyElectrical synapses are ubiquitous in interneuron networks. They form intercellular pathways, allowing electrical currents to leak between coupled interneurons. I explored the impact of electrical coupling on the integration of excitatory signals and on the coincidence detection abilities of electrically-coupled cerebellar basket cells (BCs). In order to do so, I quantified the influence of electrical coupling on the rate, the probability and the latency at which BCs generate action potentials when stimulated. The long-lasting simultaneous suprathreshold depolarization of a coupled cell evoked an increase in firing rate and a shortening of action potential latency in a reference basket cell, compared to its depolarization alone. Likewise, the action potential probability of coupled cells was strongly increased when they were simultaneously stimulated with trains of short-duration near-threshold current pulses (mimicking the activation of presynaptic granule cells) at 10 Hz, and to a lesser extent at 50 Hz, an effect that was absent in non-coupled cells. Moreover, action potential probability was increased and action potential latency was shortened in response to synaptic stimulations in mice lacking the protein that forms gap junctions between BCs, connexin36, relative to wild-type (WT) controls. These results suggest that electrical synapses between BCs decrease the probability and increase the latency of stimulus-triggered action potentials, both effects being reverted upon simultaneous excitation of coupled cells. Interestingly, varying the delay at which coupled cells are stimulated revealed that the probability and the speed of action potential generation are facilitated maximally when a basket cell is stimulated shortly after a coupled cell. These findings suggest that electrically-coupled interneurons behave as coincidence and sequence detectors that dynamically regulate the latency and the strength of inhibition onto postsynaptic targets depending on the degree of input synchrony in the coupled interneuron network.https://www.frontiersin.org/article/10.3389/fncel.2018.00156/fullgap junctionsynaptic integrationinterneuronsinhibitioncoincidencecerebellum |
| spellingShingle | Pepe Alcami Pepe Alcami Pepe Alcami Pepe Alcami Electrical Synapses Enhance and Accelerate Interneuron Recruitment in Response to Coincident and Sequential Excitation Frontiers in Cellular Neuroscience gap junction synaptic integration interneurons inhibition coincidence cerebellum |
| title | Electrical Synapses Enhance and Accelerate Interneuron Recruitment in Response to Coincident and Sequential Excitation |
| title_full | Electrical Synapses Enhance and Accelerate Interneuron Recruitment in Response to Coincident and Sequential Excitation |
| title_fullStr | Electrical Synapses Enhance and Accelerate Interneuron Recruitment in Response to Coincident and Sequential Excitation |
| title_full_unstemmed | Electrical Synapses Enhance and Accelerate Interneuron Recruitment in Response to Coincident and Sequential Excitation |
| title_short | Electrical Synapses Enhance and Accelerate Interneuron Recruitment in Response to Coincident and Sequential Excitation |
| title_sort | electrical synapses enhance and accelerate interneuron recruitment in response to coincident and sequential excitation |
| topic | gap junction synaptic integration interneurons inhibition coincidence cerebellum |
| url | https://www.frontiersin.org/article/10.3389/fncel.2018.00156/full |
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