Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum
Multiple evidence in rodents shows that the strength of excitatory synapses in the cerebral cortex and hippocampus is greater after wake than after sleep. The widespread synaptic weakening afforded by sleep is believed to keep the cost of synaptic activity under control, promote memory consolidation...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-12-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/84199 |
| _version_ | 1797975500877987840 |
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| author | Sophia S Loschky Giovanna Maria Spano William Marshall Andrea Schroeder Kelsey Marie Nemec Shannon Sandra Schiereck Luisa de Vivo Michele Bellesi Sebastian Weyn Banningh Giulio Tononi Chiara Cirelli |
| author_facet | Sophia S Loschky Giovanna Maria Spano William Marshall Andrea Schroeder Kelsey Marie Nemec Shannon Sandra Schiereck Luisa de Vivo Michele Bellesi Sebastian Weyn Banningh Giulio Tononi Chiara Cirelli |
| author_sort | Sophia S Loschky |
| collection | DOAJ |
| description | Multiple evidence in rodents shows that the strength of excitatory synapses in the cerebral cortex and hippocampus is greater after wake than after sleep. The widespread synaptic weakening afforded by sleep is believed to keep the cost of synaptic activity under control, promote memory consolidation, and prevent synaptic saturation, thus preserving the brain’s ability to learn day after day. The cerebellum is highly plastic and the Purkinje cells, the sole output neurons of the cerebellar cortex, are endowed with a staggering number of excitatory parallel fiber synapses. However, whether these synapses are affected by sleep and wake is unknown. Here, we used serial block face scanning electron microscopy to obtain the full 3D reconstruction of more than 7000 spines and their parallel fiber synapses in the mouse posterior vermis. This analysis was done in mice whose cortical and hippocampal synapses were previously measured, revealing that average synaptic size was lower after sleep compared to wake with no major changes in synapse number. Here, instead, we find that while the average size of parallel fiber synapses does not change, the number of branched synapses is reduced in half after sleep compared to after wake, corresponding to ~16% of all spines after wake and ~8% after sleep. Branched synapses are harbored by two or more spines sharing the same neck and, as also shown here, are almost always contacted by different parallel fibers. These findings suggest that during wake, coincidences of firing over parallel fibers may translate into the formation of synapses converging on the same branched spine, which may be especially effective in driving Purkinje cells to fire. By contrast, sleep may promote the off-line pruning of branched synapses that were formed due to spurious coincidences. |
| first_indexed | 2024-04-11T04:36:33Z |
| format | Article |
| id | doaj.art-19124e3371cf4ca8b43a93db043b81fb |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T04:36:33Z |
| publishDate | 2022-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-19124e3371cf4ca8b43a93db043b81fb2022-12-28T11:47:02ZengeLife Sciences Publications LtdeLife2050-084X2022-12-011110.7554/eLife.84199Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellumSophia S Loschky0Giovanna Maria Spano1https://orcid.org/0000-0003-2626-754XWilliam Marshall2Andrea Schroeder3Kelsey Marie Nemec4Shannon Sandra Schiereck5Luisa de Vivo6https://orcid.org/0000-0002-5676-9279Michele Bellesi7Sebastian Weyn Banningh8Giulio Tononi9https://orcid.org/0000-0002-3892-4087Chiara Cirelli10https://orcid.org/0000-0003-2563-677XDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United States; Department of Mathematics and Statistics, Brock University, St. Catharines, CanadaDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesDepartment of Psychiatry, University of Wisconsin-Madison, Madison, United StatesMultiple evidence in rodents shows that the strength of excitatory synapses in the cerebral cortex and hippocampus is greater after wake than after sleep. The widespread synaptic weakening afforded by sleep is believed to keep the cost of synaptic activity under control, promote memory consolidation, and prevent synaptic saturation, thus preserving the brain’s ability to learn day after day. The cerebellum is highly plastic and the Purkinje cells, the sole output neurons of the cerebellar cortex, are endowed with a staggering number of excitatory parallel fiber synapses. However, whether these synapses are affected by sleep and wake is unknown. Here, we used serial block face scanning electron microscopy to obtain the full 3D reconstruction of more than 7000 spines and their parallel fiber synapses in the mouse posterior vermis. This analysis was done in mice whose cortical and hippocampal synapses were previously measured, revealing that average synaptic size was lower after sleep compared to wake with no major changes in synapse number. Here, instead, we find that while the average size of parallel fiber synapses does not change, the number of branched synapses is reduced in half after sleep compared to after wake, corresponding to ~16% of all spines after wake and ~8% after sleep. Branched synapses are harbored by two or more spines sharing the same neck and, as also shown here, are almost always contacted by different parallel fibers. These findings suggest that during wake, coincidences of firing over parallel fibers may translate into the formation of synapses converging on the same branched spine, which may be especially effective in driving Purkinje cells to fire. By contrast, sleep may promote the off-line pruning of branched synapses that were formed due to spurious coincidences.https://elifesciences.org/articles/84199synaptic plasticitysleepelectron microscopy |
| spellingShingle | Sophia S Loschky Giovanna Maria Spano William Marshall Andrea Schroeder Kelsey Marie Nemec Shannon Sandra Schiereck Luisa de Vivo Michele Bellesi Sebastian Weyn Banningh Giulio Tononi Chiara Cirelli Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum eLife synaptic plasticity sleep electron microscopy |
| title | Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum |
| title_full | Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum |
| title_fullStr | Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum |
| title_full_unstemmed | Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum |
| title_short | Ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum |
| title_sort | ultrastructural effects of sleep and wake on the parallel fiber synapses of the cerebellum |
| topic | synaptic plasticity sleep electron microscopy |
| url | https://elifesciences.org/articles/84199 |
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