Abstract
In this article, we review studies of astrocytic-neuronal interactions and their effects on the activity of oxytocin (OXT) neurons within the magnocellular hypothalamo-neurohypophysial system. Previous work over several decades has shown that withdrawal of astrocyte processes increases OXT neuron excitability in the hypothalamic supraoptic nucleus (SON) during lactation. However, chronically disabling astrocyte withdrawal does not significantly affect the functioning of OXT neurons during suckling. Nevertheless, acute changes in a cytoskeletal element of astrocytes, glial fibrillary acidic protein (GFAP), occur in concert with changes in OXT neuronal activity during suckling. Here, we compare these changes in GFAP and related proteins with chronic changes that persist throughout lactation. During lactation, a decrease in GFAP levels accompanies retraction of astrocyte processes surrounding OXT neurons in the SON, resulting from high extracellular levels of OXT. During the initial stage of suckling, acute increases in OXT levels further strengthen this GFAP reduction and facilitate the retraction of astrocyte processes. This change, in turn, facilitates burst discharges of OXT neurons and leads to a transient increase in excitatory neurochemicals. This transient neurochemical surge acts to reverse GFAP expression and results in postburst inhibition of OXT neurons. The acute changes in astrocyte GFAP levels seen during suckling likely recur periodically, accompanied by rhythmic changes in glutamate metabolism, water transport, gliotransmitter release, and spatial relationships between astrocytes and OXT neurons. In the neurohypophysis, astrocyte retraction and reversal with accompanying GFAP plasticity also likely occur during lactation and suckling, which facilitates OXT release coordinated with its action in the SON. These studies of the dynamic interactions that occur between astrocytes and OXT neurons mediated by GFAP extend our understanding of astrocyte functions within the central nervous system.
Highlights
CHRONIC INTERACTIONS BETWEEN ASTROCYTES AND OXT NEURONSThe influence of astrocytes on neuronal activity largely depends on changes in astrocyte morphology and functions that are induced by neuronal activity
Morphological and functional plasticity of astrocytes plays an important role in modulating neuronal activity
We focus on acute changes in glial fibrillary acidic protein (GFAP, an astrocyte cytoskeletal element) and its interaction with associated molecules that affect the functioning of the magnocellular hypothalamoneurohypophysial system during suckling
Summary
The influence of astrocytes on neuronal activity largely depends on changes in astrocyte morphology and functions that are induced by neuronal activity. During the late stage of pregnancy and lactation, astrocyte processes, together with their GFAP content, withdraw from the OXT neurons[9], which increases direct neuronal apposition This change facilitates formation of gap junctions and rapid communication between apposed neurons. It is likely that astrocyte retraction in the SON results in increased levels of extracellular K+, glutamate, and other neurochemicals, and in increased neuronal coupling[14,15], which together facilitate the coordinated burst firing of magnocellular neurons[16] This burst firing, in turn, maximizes release of OXT from the neurohypophysis[17], which triggers milk ejection by eliciting contraction of the mammary myoepithelium. The failure of endoneuraminidase to block activation of OXT neurons suggests that chronic retraction of astrocyte processes is not essential to astrocyte-mediated modulation of OXT neuronal activity
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