Functional Rhythmogenic Domains Defined by Astrocytic Networks in the Trigeminal Main Sensory Nucleus.
Glia. 2017-10-23; 66(2): 311-326
DOI: 10.1002/glia.23244
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Stimuli that induce rhythmic firing in trigeminal neurons also increase
astrocytic coupling and reveal networks that define the boundaries of this
particular population. Rhythmic firing depends on astrocytic coupling which in
turn depends on S100β. In many nervous functions that rely on the ability of
neuronal networks to generate a rhythmic pattern of activity, coordination of
firing is an essential feature. Astrocytes play an important role in some of
these networks, but the contribution of astrocytic coupling remains poorly
defined. Here we investigate the modulation and organization of astrocytic
networks in the dorsal part of the trigeminal main sensory nucleus (NVsnpr),
which forms part of the network generating chewing movements. Using whole-cell
recordings and the dye coupling approach by filling a single astrocyte with
biocytin to reveal astrocytic networks, we showed that coupling is limited under
resting conditions, but increases importantly under conditions that induce
rhythmic firing in NVsnpr neurons. These are: repetitive electrical stimulation
of the sensory inputs to the nucleus, local application of NMDA and decrease of
extracellular Ca2+ . We have previously shown that rhythmic firing induced in
NVsnpr neurons by these stimuli depends on astrocytes and their Ca2+ -binding
protein S100β. Here we show that extracellular blockade of S100β also prevents
the increase in astrocytic coupling induced by local application of NMDA. Most of
the networks were small and remained confined to the functionally distinct area
of dorsal NVsnpr. Disrupting coupling by perfusion with the nonspecific gap
junction blocker, carbenoxolone or with GAP26, a selective inhibitor of connexin
43, mostly expressed in astrocytes, abolished NMDA-induced rhythmic firing in
NVsnpr neurons. These results suggest that astrocytic coupling is regulated by
sensory inputs, necessary for neuronal bursting, and organized in a region
specific manner.