Somatic Cx36 gap junctions expand the anatomical substrate for electrical coupling in the adult mouse inferior olive

Abstract

The inferior olive (IO) is unique among adult mammalian brain nuclei in that its neurons communicate solely via gap junctions. For more than half a century, models of cerebellar timing, synchrony, and learning have therefore centered on how electrical coupling between olivary neurons is regulated. In the prevailing anatomical model, IO gap junctions reside on dendritic spines within olivary glomeruli, where nearby inhibitory terminals can locally regulate coupling through shunting conductances. Here we show that this view is incomplete. In the adult mouse IO, closely apposed neuronal somata are common, direct soma-soma appositions are visible by volume electron microscopy, Cx36 puncta occur at somatic contacts, and freeze-fracture replica labeling identifies Cx36-associated gap junction plaques on large continuous membrane surfaces. These soma-proximal gap junctions extend olivary electrical coupling beyond dendritic-spine glomeruli, challenging a core anatomical assumption in models of cerebellar coordination.