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Front. Cell. Neurosci. | doi: 10.3389/fncel.2018.00431

Anisotropic panglial coupling reflects tonotopic organization in the inferior colliculus

Simon L. Wadle1, Vanessa Augustin1, Julia Langer2, Ronald Jabs3, Camille Philippot3, Dennis J. Weingarten1,  Christine R. Rose2, Christian Steinhäuser3 and  Jonathan Stephan1*
  • 1Department of Biology , Animal Physiology Group, Technische Universität Kaiserslautern, Germany
  • 2Institute of Neurobiology, Heinrich Heine Universität Düsseldorf, Germany
  • 3Medical Faculty , Institute of Cellular Neurosciences, Universität Bonn, Germany

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.

Keywords: Astrocytes, oligodendrocytes, auditory brainstem, IC, Gap Junctions, Connexin 43, Connexin 30

Received: 01 Aug 2018; Accepted: 31 Oct 2018.

Edited by:

Juan A. Orellana, Pontificia Universidad Católica de Chile, Chile

Reviewed by:

Georg Zoidl, York University, Canada
Eliseo A. Eugenin, The University of Texas Medical Branch at Galveston, United States  

Copyright: © 2018 Wadle, Augustin, Langer, Jabs, Philippot, Weingarten, Rose, Steinhäuser and Stephan. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Jonathan Stephan, Technische Universität Kaiserslautern, Department of Biology , Animal Physiology Group, Kaiserslautern, 67663, Rhineland-Palatinate, Germany, jonathan.stephan@bio.uni-kl.de