Functional anisotropic panglial networks in the lateral superior olive

Abstract

Astrocytes form large gap junctional networks that contribute to ion and neurotransmitter homeostasis. Astrocytes concentrate in the lateral superior olive (LSO), a prominent auditory brainstem center. Compared to the LSO, astrocyte density is lower in the region dorsal to the LSO (dLSO) and in the internuclear space between the LSO, the superior paraolivary nucleus (SPN). We questioned whether astrocyte networks exhibit certain properties that reflect the precise neuronal arrangement. Employing whole-cell patch-clamp and concomitant injection of a gap junction-permeable tracer, we analyzed size and orientation of astrocyte networks in LSO, dLSO, and SPN-LSO in acute brainstem slices of mice at postnatal days 10-20. The majority of LSO networks exhibited an oval topography oriented orthogonally to the tonotopic axis, whereas dLSO networks showed no preferred orientation. This correlated with the overall astrocyte morphology in both regions, i.e. LSO astrocyte processes were oriented mainly orthogonally to the tonotopic axis. To assess the spread of small ions within LSO networks, we analyzed the diffusion of Na(+) signals between cells using Na(+) imaging. We found that Na(+) not only diffused between SR101(+) astrocytes, but also from astrocytes into SR101(-) cells. Using PLP-GFP mice for tracing, we could show that LSO networks contained astrocytes and oligodendrocytes. Together, our results demonstrate that LSO astrocytes and LSO oligodendrocytes form functional anisotropic panglial networks that are oriented predominantly orthogonally to the tonotopic axis. Thus, our results point toward an anisotropic ion and metabolite diffusion and a limited glial crosstalk between neighboring isofrequency bands in the LSO. GLIA 2016;64:1892-1911.

Ionic signalling in astroglia beyond calcium

“…This type of inter‐glial communication was identified in grey as well as in white matter (Augustin et al . ; Moshrefi‐Ravasdjani et al . ).…”

Altered Gap Junction Network Topography in Mouse Models for Human Hereditary Deafness

“…In many brain regions, astrocytes and oligodendrocytes form large panglial gap junction (GJ)-mediated networks [ 1 , 2 , 3 , 4 ]. In the hippocampus, where only few oligodendrocytes are located [ 1 , 5 ], networks mainly consist of astrocytes [ 6 ]. GJ networks exhibit a heterogeneous topography throughout the CNS.…”

“…In the barrel cortex and the barreloid thalamus, tracer coupling is restricted to the barrels [ 7 , 8 ]. Moreover, anisotropic tracer spread is present in the lateral superior olive (LSO) and the inferior colliculus (IC) [ 1 , 2 , 9 ]—two nuclei of the auditory brainstem, in which tracer-coupled networks are oriented orthogonally to the tonotopic axis. Both LSO and IC are tonotopically organized [ 10 , 11 , 12 ] and principal neurons refer to this organization, as their dendritic trees exhibit a narrow morphology with an orientation orthogonal to the tonotopic axis [ 13 , 14 , 15 , 16 , 17 ].…”

Oligodendrocytes Remodel the Genomic Fabrics of Functional Pathways in Astrocytes

“…Gap junctions provide a two-way route for interaction between oligodendrocytes and astrocytes [4][5][6], where specific connexin proteins form the intercellular channels in the different cells. Astrocytes express Cx43 (Gja1) and Cx30 (Gjb6), whereas oligodendrocytes express Cx32 (Gjb1) and Cx47 (Gja12), and the two cell types communicate through heterotypic connexin pairing.…”