Panglial gap junctions between astrocytes and olfactory ensheathing cells mediate transmission of Ca2+ transients and neurovascular coupling

Abstract

Astrocytes are arranged in highly organized gap junction-coupled networks, communicating via the propagation of Ca2+ waves. Astrocytes are gap junction-coupled not only to neighboring astrocytes, but also to oligodendrocytes, forming so-called panglial syncytia. It is not known, however, whether glial cells in panglial syncytia transmit information using Ca2+ signaling. We used confocal Ca2+ imaging to study intercellular communication between astrocytes and olfactory ensheathing glial cells (OECs) in in-toto preparations of the mouse olfactory bulb. Our results demonstrate that Ca2+ transients in juxtaglomerular astrocytes, evoked by local photolysis of “caged” ATP and “caged” tACPD, led to subsequent Ca2+ responses in OECs. This transmission of Ca2+ responses from astrocytes to OECs persisted in the presence of neuronal inhibition, but was absent when gap junctional coupling was suppressed with carbenoxolone. When Ca2+ transients were directly evoked in OECs by puff application of DHPG, they resulted in delayed Ca2+ responses in juxtaglomerular astrocytes, indicating that panglial transmission of Ca2+ signals occurred in a bidirectional manner. In addition, panglial transmission of Ca2+ signals from astrocytes to OECs resulted in vasoconstriction of OEC-associated blood vessels in the olfactory nerve layer. Our results demonstrate functional transmission of Ca2+ signals between different classes of glial cells within gap junction-coupled panglial networks and the resulting regulation of blood vessel diameter in the olfactory bulb.