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Cytoarchitectural analysis of the neuron-to-glia association in the dorsal root ganglia of normal and diabetic mice

Abstract: Dorsal root ganglia (DRGs) host the somata of sensory neurons which convey information from the periphery to the central nervous system. These neurons have heterogeneous size and neurochemistry, and those of small-to-medium size, which play an important role in nociception, form two distinct subpopulations based on the presence (peptidergic) or absence (non-peptidergic) of transmitter neuropeptides. Few investigations have so far addressed the spatial relationship between neurochemically different subpopulations of DRG neurons and glia. We used a whole-mount mouse lumbar DRG preparation, confocal microscopy and computer-aided 3D analysis to unveil that IB4+ non-peptidergic neurons form small clusters of 4.7 ± 0.26 cells, differently from CGRP+ peptidergic neurons that are, for the most, isolated (1.89 ± 0.11 cells). Both subpopulations of neurons are ensheathed by a thin layer of satellite glial cells (SGCs) that can be observed after immunolabeling with the specific marker glutamine synthetase (GS). Notably, at the ultrastructural level we observed that this glial layer was discontinuous, as there were patches of direct contact between the membranes of two adjacent IB4+ neurons. To test whether this cytoarchitectonic organization was modified in the diabetic neuropathy, one of the most devastating sensory pathologies, mice were made diabetic by streptozotocin (STZ). In diabetic animals, cluster organization of the IB4+ non-peptidergic neurons was maintained, but the neuro-glial relationship was altered, as STZ treatment caused a statistically significant increase of GS staining around CGRP+ neurons but a reduction around IB4+ neurons. Ultrastructural analysis unveiled that SGC coverage was increased at the interface between IB4+ cluster-forming neurons in diabetic mice, with a 50% reduction in the points of direct contacts between cells. These observations demonstrate the existence of a structural plasticity of the DRG cytoarchitecture in response to STZ.


Citation:

Ciglieri, Elisa; Vacca, Maurizia; Ferrini, Francesco; Atteya, Mona A; Aimar, Patrizia; Ficarra, Elisa; Di Cataldo, Santa; Merighi, Adalberto; Salio, Chiara "Cytoarchitectural analysis of the neuron-to-glia association in the dorsal root ganglia of normal and diabetic mice" JOURNAL OF ANATOMY, vol. 237, pp. 988 -997 , 2020 DOI: 10.1111/joa.13252

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