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Action potential counting at giant mossy fiber terminals gates information transfer in the hippocampus
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Chamberland, Simon, Timofeeva, Yulia, Evstratova, Alesya, Volynski, Kirill and Tóth, Katalin (2018) Action potential counting at giant mossy fiber terminals gates information transfer in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 115 (28). pp. 7434-7439. doi:10.1073/pnas.1720659115 ISSN 0027-8424.
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WRAP-action-potential-counting-giant-mossy-fiber-gates-hippocampus-Timofeeva-2018.pdf - Published Version - Requires a PDF viewer. Available under License Creative Commons Attribution Non-commercial No Derivatives 4.0. Download (1531Kb) | Preview |
Official URL: http://doi.org/10.1073/pnas.1720659115
Abstract
Neuronal communication relies on action potential discharge, with the frequency and the temporal precision of action potentials encoding information. Hippocampal mossy fibers have long been recognized as conditional detonators owing to prominent short-term facilitation of glutamate release displayed during granule cell burst firing. However, the spiking patterns required to trigger action potential firing in CA3 pyramidal neurons remain poorly understood. Here, we show that glutamate release from mossy fiber terminals triggers action potential firing of the target CA3 pyramidal neurons independently of the average granule cell burst frequency, a phenomenon we term action potential counting. We find that action potential counting in mossy fibers gates glutamate release over a broad physiological range of frequencies and action potential numbers. Using rapid Ca imaging we also show that the magnitude of evoked Ca influx stays constant during action potential trains and that accumulated residual Ca is gradually extruded on a time scale of several hundred milliseconds. Using experimentally constrained 3D model of presynaptic Ca influx, buffering, and diffusion, and a Monte Carlo model of Ca -activated vesicle fusion, we argue that action potential counting at mossy fiber boutons can be explained by a unique interplay between Ca dynamics and buffering at release sites. This is largely determined by the differential contribution of major endogenous Ca buffers calbindin-D and calmodulin and by the loose coupling between presynaptic voltage-gated Ca channels and release sensors and the relatively slow Ca extrusion rate. Taken together, our results identify a previously unexplored information-coding mechanism in the brain.
| Item Type: | Journal Article | ||||||||||||||||||
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| Subjects: | R Medicine > RC Internal medicine > RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry | ||||||||||||||||||
| Divisions: | Faculty of Science, Engineering and Medicine > Research Centres > Centre for Complexity Science Faculty of Science, Engineering and Medicine > Science > Computer Science |
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| SWORD Depositor: | Library Publications Router | ||||||||||||||||||
| Library of Congress Subject Headings (LCSH): | Hippocampus (Brain), Neurons, Presynaptic receptor | ||||||||||||||||||
| Journal or Publication Title: | Proceedings of the National Academy of Sciences of the United States of America | ||||||||||||||||||
| Publisher: | National Academy of Sciences | ||||||||||||||||||
| ISSN: | 0027-8424 | ||||||||||||||||||
| Official Date: | 10 July 2018 | ||||||||||||||||||
| Dates: |
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| Volume: | 115 | ||||||||||||||||||
| Number: | 28 | ||||||||||||||||||
| Page Range: | pp. 7434-7439 | ||||||||||||||||||
| DOI: | 10.1073/pnas.1720659115 | ||||||||||||||||||
| Status: | Peer Reviewed | ||||||||||||||||||
| Publication Status: | Published | ||||||||||||||||||
| Access rights to Published version: | Open Access (Creative Commons) | ||||||||||||||||||
| Date of first compliant deposit: | 18 July 2018 | ||||||||||||||||||
| Date of first compliant Open Access: | 18 July 2018 | ||||||||||||||||||
| RIOXX Funder/Project Grant: |
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