Medullary Respiratory Circuit Is Reorganized by a Seasonally-Induced Program in Preparation for Hibernation
Deep hibernators go through several cycles of profound drops in body temperature during the winter season, with core temperatures sometimes reaching near freezing. Yet unlike non-hibernating mammals, they can sustain breathing rhythms. The physiological processes that make this possible are still no...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-04-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnins.2019.00376/full |
| _version_ | 1818542987159797760 |
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| author | Thomas L. Russell Jichang Zhang Michal Okoniewski Felix Franke Sandrine Bichet Andreas Hierlemann |
| author_facet | Thomas L. Russell Jichang Zhang Michal Okoniewski Felix Franke Sandrine Bichet Andreas Hierlemann |
| author_sort | Thomas L. Russell |
| collection | DOAJ |
| description | Deep hibernators go through several cycles of profound drops in body temperature during the winter season, with core temperatures sometimes reaching near freezing. Yet unlike non-hibernating mammals, they can sustain breathing rhythms. The physiological processes that make this possible are still not understood. In this study, we focused on the medullary Ventral Respiratory Column of a facultative hibernator, the Syrian hamster. Using shortened day-lengths, we induced a “winter-adapted” physiological state, which is a prerequisite for hibernation. When recording electrophysiological signals from acute slices in the winter-adapted pre-Bötzinger complex (preBötC), spike trains showed higher spike rates, amplitudes, complexity, as well as higher temperature sensitivity, suggesting an increase in connectivity and/or synaptic strength during the winter season. We further examined action potential waveforms and found that the depolarization integral, as measured by the area under the curve, is selectively enhanced in winter-adapted animals. This suggests that a shift in the ion handling kinetics is also being induced by the winter-adaptation program. RNA sequencing of respiratory pre-motor neurons, followed by gene set enrichment analysis, revealed differential regulation and splicing in structural, synaptic, and ion handling genes. Splice junction analysis suggested that differential exon usage is occurring in a select subset of ion handling subunits (ATP1A3, KCNC3, SCN1B), and synaptic structure genes (SNCB, SNCG, RAB3A). Our findings show that the hamster respiratory center undergoes a seasonally-cued alteration in electrophysiological properties, likely protecting against respiratory failure at low temperatures. |
| first_indexed | 2024-12-11T22:29:22Z |
| format | Article |
| id | doaj.art-583f1f1e7e3a4185bc8635bceaea20a4 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-12-11T22:29:22Z |
| publishDate | 2019-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-583f1f1e7e3a4185bc8635bceaea20a42022-12-22T00:48:11ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-04-011310.3389/fnins.2019.00376439772Medullary Respiratory Circuit Is Reorganized by a Seasonally-Induced Program in Preparation for HibernationThomas L. Russell0Jichang Zhang1Michal Okoniewski2Felix Franke3Sandrine Bichet4Andreas Hierlemann5Department of Biosystems Science and Engineering, ETH Zürich, Basel, SwitzerlandDepartment of Biosystems Science and Engineering, ETH Zürich, Basel, SwitzerlandScientific IT Services, ETH Zurich, Zurich, SwitzerlandDepartment of Biosystems Science and Engineering, ETH Zürich, Basel, SwitzerlandFriedrich Miescher Institute for Biomedical Research, Department of Histology, Basel, SwitzerlandDepartment of Biosystems Science and Engineering, ETH Zürich, Basel, SwitzerlandDeep hibernators go through several cycles of profound drops in body temperature during the winter season, with core temperatures sometimes reaching near freezing. Yet unlike non-hibernating mammals, they can sustain breathing rhythms. The physiological processes that make this possible are still not understood. In this study, we focused on the medullary Ventral Respiratory Column of a facultative hibernator, the Syrian hamster. Using shortened day-lengths, we induced a “winter-adapted” physiological state, which is a prerequisite for hibernation. When recording electrophysiological signals from acute slices in the winter-adapted pre-Bötzinger complex (preBötC), spike trains showed higher spike rates, amplitudes, complexity, as well as higher temperature sensitivity, suggesting an increase in connectivity and/or synaptic strength during the winter season. We further examined action potential waveforms and found that the depolarization integral, as measured by the area under the curve, is selectively enhanced in winter-adapted animals. This suggests that a shift in the ion handling kinetics is also being induced by the winter-adaptation program. RNA sequencing of respiratory pre-motor neurons, followed by gene set enrichment analysis, revealed differential regulation and splicing in structural, synaptic, and ion handling genes. Splice junction analysis suggested that differential exon usage is occurring in a select subset of ion handling subunits (ATP1A3, KCNC3, SCN1B), and synaptic structure genes (SNCB, SNCG, RAB3A). Our findings show that the hamster respiratory center undergoes a seasonally-cued alteration in electrophysiological properties, likely protecting against respiratory failure at low temperatures.https://www.frontiersin.org/article/10.3389/fnins.2019.00376/fullmicroelectrode arrayelectrophysiologyhibernationrespiratory rhythmsventral respiratory groupmedulla |
| spellingShingle | Thomas L. Russell Jichang Zhang Michal Okoniewski Felix Franke Sandrine Bichet Andreas Hierlemann Medullary Respiratory Circuit Is Reorganized by a Seasonally-Induced Program in Preparation for Hibernation Frontiers in Neuroscience microelectrode array electrophysiology hibernation respiratory rhythms ventral respiratory group medulla |
| title | Medullary Respiratory Circuit Is Reorganized by a Seasonally-Induced Program in Preparation for Hibernation |
| title_full | Medullary Respiratory Circuit Is Reorganized by a Seasonally-Induced Program in Preparation for Hibernation |
| title_fullStr | Medullary Respiratory Circuit Is Reorganized by a Seasonally-Induced Program in Preparation for Hibernation |
| title_full_unstemmed | Medullary Respiratory Circuit Is Reorganized by a Seasonally-Induced Program in Preparation for Hibernation |
| title_short | Medullary Respiratory Circuit Is Reorganized by a Seasonally-Induced Program in Preparation for Hibernation |
| title_sort | medullary respiratory circuit is reorganized by a seasonally induced program in preparation for hibernation |
| topic | microelectrode array electrophysiology hibernation respiratory rhythms ventral respiratory group medulla |
| url | https://www.frontiersin.org/article/10.3389/fnins.2019.00376/full |
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