Artificial sleep-like up/down-states induce synaptic plasticity in cortical neurons from mouse brain slices
During non-rapid eye movement (NREM) sleep, cortical neuron activity alternates between a depolarized (firing, up-state) and a hyperpolarized state (down-state) coinciding with delta electroencephalogram (EEG) slow-wave oscillation (SWO, 0. 5–4 Hz) in vivo. Recently, we have found that artificial sl...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-10-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncel.2022.948327/full |
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| author | Gai-Linn Kay Besing Emily Kate St. John Cobie Victoria Potesta Martin J. Gallagher Martin J. Gallagher Chengwen Zhou Chengwen Zhou |
| author_facet | Gai-Linn Kay Besing Emily Kate St. John Cobie Victoria Potesta Martin J. Gallagher Martin J. Gallagher Chengwen Zhou Chengwen Zhou |
| author_sort | Gai-Linn Kay Besing |
| collection | DOAJ |
| description | During non-rapid eye movement (NREM) sleep, cortical neuron activity alternates between a depolarized (firing, up-state) and a hyperpolarized state (down-state) coinciding with delta electroencephalogram (EEG) slow-wave oscillation (SWO, 0. 5–4 Hz) in vivo. Recently, we have found that artificial sleep-like up/down-states can potentiate synaptic strength in layer V cortical neurons ex vivo. Using mouse coronal brain slices, whole cell voltage-clamp recordings were made from layer V cortical pyramidal neurons to record spontaneous excitatory synaptic currents (sEPSCs) and inhibitory synaptic currents (sIPSCs). Artificial sleep-like up/down-states (as SWOs, 0.5 Hz, 10 min, current clamp mode) were induced by injecting sinusoidal currents into layer V cortical neurons. Baseline pre-SWO recordings were recorded for 5 min and post-SWO recordings for at least 25–30 min. Compared to pre-SWO sEPSCs or sIPSCs, post-SWO sEPSCs or sIPSCs in layer V cortical neurons exhibited significantly larger amplitudes and a higher frequency for 30 min. This finding suggests that both sEPSCs and sIPSCs could be potentiated in layer V cortical neurons by the low-level activity of SWOs, and sEPSCs and sIPSCs maintained a balance in layer V cortical neurons during pre- and post-SWO periods. Overall, this study presents an ex vivo method to show SWO's ability to induce synaptic plasticity in layer V cortical neurons, which may underlie sleep-related synaptic potentiation for sleep-related memory consolidation in vivo. |
| first_indexed | 2024-04-11T16:50:18Z |
| format | Article |
| id | doaj.art-c3a3cd89399f454f9c730d4bc8053b77 |
| institution | Directory Open Access Journal |
| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-04-11T16:50:18Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-c3a3cd89399f454f9c730d4bc8053b772022-12-22T04:13:28ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022022-10-011610.3389/fncel.2022.948327948327Artificial sleep-like up/down-states induce synaptic plasticity in cortical neurons from mouse brain slicesGai-Linn Kay Besing0Emily Kate St. John1Cobie Victoria Potesta2Martin J. Gallagher3Martin J. Gallagher4Chengwen Zhou5Chengwen Zhou6Departments of Neurology, Vanderbilt University Medical Center, Nashville, TN, United StatesDepartments of Neurology, Vanderbilt University Medical Center, Nashville, TN, United StatesDepartments of Neurology, Vanderbilt University Medical Center, Nashville, TN, United StatesDepartments of Neurology, Vanderbilt University Medical Center, Nashville, TN, United StatesNeuroscience Graduate Program, Vanderbilt University Medical Center, Nashville, TN, United StatesDepartments of Neurology, Vanderbilt University Medical Center, Nashville, TN, United StatesNeuroscience Graduate Program, Vanderbilt University Medical Center, Nashville, TN, United StatesDuring non-rapid eye movement (NREM) sleep, cortical neuron activity alternates between a depolarized (firing, up-state) and a hyperpolarized state (down-state) coinciding with delta electroencephalogram (EEG) slow-wave oscillation (SWO, 0. 5–4 Hz) in vivo. Recently, we have found that artificial sleep-like up/down-states can potentiate synaptic strength in layer V cortical neurons ex vivo. Using mouse coronal brain slices, whole cell voltage-clamp recordings were made from layer V cortical pyramidal neurons to record spontaneous excitatory synaptic currents (sEPSCs) and inhibitory synaptic currents (sIPSCs). Artificial sleep-like up/down-states (as SWOs, 0.5 Hz, 10 min, current clamp mode) were induced by injecting sinusoidal currents into layer V cortical neurons. Baseline pre-SWO recordings were recorded for 5 min and post-SWO recordings for at least 25–30 min. Compared to pre-SWO sEPSCs or sIPSCs, post-SWO sEPSCs or sIPSCs in layer V cortical neurons exhibited significantly larger amplitudes and a higher frequency for 30 min. This finding suggests that both sEPSCs and sIPSCs could be potentiated in layer V cortical neurons by the low-level activity of SWOs, and sEPSCs and sIPSCs maintained a balance in layer V cortical neurons during pre- and post-SWO periods. Overall, this study presents an ex vivo method to show SWO's ability to induce synaptic plasticity in layer V cortical neurons, which may underlie sleep-related synaptic potentiation for sleep-related memory consolidation in vivo.https://www.frontiersin.org/articles/10.3389/fncel.2022.948327/fullhomeostatic synaptic plasticitybrain slicessleepup/down-statewhole-cell recordings |
| spellingShingle | Gai-Linn Kay Besing Emily Kate St. John Cobie Victoria Potesta Martin J. Gallagher Martin J. Gallagher Chengwen Zhou Chengwen Zhou Artificial sleep-like up/down-states induce synaptic plasticity in cortical neurons from mouse brain slices Frontiers in Cellular Neuroscience homeostatic synaptic plasticity brain slices sleep up/down-state whole-cell recordings |
| title | Artificial sleep-like up/down-states induce synaptic plasticity in cortical neurons from mouse brain slices |
| title_full | Artificial sleep-like up/down-states induce synaptic plasticity in cortical neurons from mouse brain slices |
| title_fullStr | Artificial sleep-like up/down-states induce synaptic plasticity in cortical neurons from mouse brain slices |
| title_full_unstemmed | Artificial sleep-like up/down-states induce synaptic plasticity in cortical neurons from mouse brain slices |
| title_short | Artificial sleep-like up/down-states induce synaptic plasticity in cortical neurons from mouse brain slices |
| title_sort | artificial sleep like up down states induce synaptic plasticity in cortical neurons from mouse brain slices |
| topic | homeostatic synaptic plasticity brain slices sleep up/down-state whole-cell recordings |
| url | https://www.frontiersin.org/articles/10.3389/fncel.2022.948327/full |
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