Anisotropic Panglial Coupling Reflects Tonotopic Organization in the Inferior Colliculus
Astrocytes and oligodendrocytes in different brain regions form panglial networks and the topography of such networks can correlate with neuronal topography and function. Astrocyte-oligodendrocyte networks in the lateral superior olive (LSO)—an auditory brainstem nucleus—were found to be anisotropic...
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Frontiers Media S.A.
2018-11-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fncel.2018.00431/full |
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| author | Simon L. Wadle Vanessa Augustin Julia Langer Ronald Jabs Camille Philippot Dennis J. Weingarten Christine R. Rose Christian Steinhäuser Jonathan Stephan |
| author_facet | Simon L. Wadle Vanessa Augustin Julia Langer Ronald Jabs Camille Philippot Dennis J. Weingarten Christine R. Rose Christian Steinhäuser Jonathan Stephan |
| author_sort | Simon L. Wadle |
| collection | DOAJ |
| description | Astrocytes and oligodendrocytes in different brain regions form panglial networks and the topography of such networks can correlate with neuronal topography and function. Astrocyte-oligodendrocyte networks in the lateral superior olive (LSO)—an auditory brainstem nucleus—were found to be anisotropic with a preferred orientation orthogonally to the tonotopic axis. We hypothesized that such a specialization might be present in other tonotopically organized brainstem nuclei, too. Thus, we analyzed gap junctional coupling in the center of the inferior colliculus (IC)—another nucleus of the auditory brainstem that exhibits tonotopic organization. In acute brainstem slices obtained from mice, IC networks were traced employing whole-cell patch-clamp recordings of single sulforhodamine (SR) 101-identified astrocytes and concomitant intracellular loading of the gap junction-permeable tracer neurobiotin. The majority of dye-coupled networks exhibited an oval topography, which was preferentially oriented orthogonal to the tonotopic axis. Astrocyte processes showed preferentially the same orientation indicating a correlation between astrocyte and network topography. In addition to SR101-positive astrocytes, IC networks contained oligodendrocytes. Using Na+ imaging, we analyzed the capability of IC networks to redistribute small ions. Na+ bi-directionally diffused between SR101-positive astrocytes and SR101-negative cells—presumably oligodendrocytes—showing the functionality of IC networks. Taken together, our results demonstrate that IC astrocytes and IC oligodendrocytes form functional anisotropic panglial networks that are preferentially oriented orthogonal to the tonotopic axis. Thus, our data indicate that the topographic specialization of glial networks seen in IC and LSO might be a general feature of tonotopically organized auditory brainstem nuclei. |
| first_indexed | 2024-04-13T02:01:19Z |
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| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-04-13T02:01:19Z |
| publishDate | 2018-11-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-22518b20a82c460d868fe38992491be72022-12-22T03:07:37ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022018-11-011210.3389/fncel.2018.00431417403Anisotropic Panglial Coupling Reflects Tonotopic Organization in the Inferior ColliculusSimon L. Wadle0Vanessa Augustin1Julia Langer2Ronald Jabs3Camille Philippot4Dennis J. Weingarten5Christine R. Rose6Christian Steinhäuser7Jonathan Stephan8Animal Physiology Group, Department of Biology, University of Kaiserslautern, Kaiserslautern, GermanyAnimal Physiology Group, Department of Biology, University of Kaiserslautern, Kaiserslautern, GermanyInstitute of Neurobiology, Heinrich Heine University Düsseldorf, Düsseldorf, GermanyInstitute of Cellular Neurosciences, Medical Faculty, University of Bonn, Bonn, GermanyInstitute of Cellular Neurosciences, Medical Faculty, University of Bonn, Bonn, GermanyAnimal Physiology Group, Department of Biology, University of Kaiserslautern, Kaiserslautern, GermanyInstitute of Neurobiology, Heinrich Heine University Düsseldorf, Düsseldorf, GermanyInstitute of Cellular Neurosciences, Medical Faculty, University of Bonn, Bonn, GermanyAnimal Physiology Group, Department of Biology, University of Kaiserslautern, Kaiserslautern, GermanyAstrocytes and oligodendrocytes in different brain regions form panglial networks and the topography of such networks can correlate with neuronal topography and function. Astrocyte-oligodendrocyte networks in the lateral superior olive (LSO)—an auditory brainstem nucleus—were found to be anisotropic with a preferred orientation orthogonally to the tonotopic axis. We hypothesized that such a specialization might be present in other tonotopically organized brainstem nuclei, too. Thus, we analyzed gap junctional coupling in the center of the inferior colliculus (IC)—another nucleus of the auditory brainstem that exhibits tonotopic organization. In acute brainstem slices obtained from mice, IC networks were traced employing whole-cell patch-clamp recordings of single sulforhodamine (SR) 101-identified astrocytes and concomitant intracellular loading of the gap junction-permeable tracer neurobiotin. The majority of dye-coupled networks exhibited an oval topography, which was preferentially oriented orthogonal to the tonotopic axis. Astrocyte processes showed preferentially the same orientation indicating a correlation between astrocyte and network topography. In addition to SR101-positive astrocytes, IC networks contained oligodendrocytes. Using Na+ imaging, we analyzed the capability of IC networks to redistribute small ions. Na+ bi-directionally diffused between SR101-positive astrocytes and SR101-negative cells—presumably oligodendrocytes—showing the functionality of IC networks. Taken together, our results demonstrate that IC astrocytes and IC oligodendrocytes form functional anisotropic panglial networks that are preferentially oriented orthogonal to the tonotopic axis. Thus, our data indicate that the topographic specialization of glial networks seen in IC and LSO might be a general feature of tonotopically organized auditory brainstem nuclei.https://www.frontiersin.org/article/10.3389/fncel.2018.00431/fullastrocytesoligodendrocytesauditory brainstemICgap junctionsconnexin 43 |
| spellingShingle | Simon L. Wadle Vanessa Augustin Julia Langer Ronald Jabs Camille Philippot Dennis J. Weingarten Christine R. Rose Christian Steinhäuser Jonathan Stephan Anisotropic Panglial Coupling Reflects Tonotopic Organization in the Inferior Colliculus Frontiers in Cellular Neuroscience astrocytes oligodendrocytes auditory brainstem IC gap junctions connexin 43 |
| title | Anisotropic Panglial Coupling Reflects Tonotopic Organization in the Inferior Colliculus |
| title_full | Anisotropic Panglial Coupling Reflects Tonotopic Organization in the Inferior Colliculus |
| title_fullStr | Anisotropic Panglial Coupling Reflects Tonotopic Organization in the Inferior Colliculus |
| title_full_unstemmed | Anisotropic Panglial Coupling Reflects Tonotopic Organization in the Inferior Colliculus |
| title_short | Anisotropic Panglial Coupling Reflects Tonotopic Organization in the Inferior Colliculus |
| title_sort | anisotropic panglial coupling reflects tonotopic organization in the inferior colliculus |
| topic | astrocytes oligodendrocytes auditory brainstem IC gap junctions connexin 43 |
| url | https://www.frontiersin.org/article/10.3389/fncel.2018.00431/full |
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