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The Journal of Neuroscience, February 11, 2009, 29(6):1743-1754; doi:10.1523/JNEUROSCI.4669-08.2009

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Cellular/Molecular
Astrocytic Plasticity and Patterned Oxytocin Neuronal Activity: Dynamic Interactions

Yu-Feng Wang and Glenn I. Hatton

Department of Cell Biology and Neuroscience, University of California, Riverside, California 92521

Correspondence should be addressed to Glenn I. Hatton, Department of Cell Biology and Neuroscience, University of California, Riverside, CA 92521. Email: glenn.hatton{at}ucr.edu

Astroglial–neuronal interactions are important in brain functions. However, roles of glial fibrillary acidic protein (GFAP) in this interaction remain unclear in acute physiological processes. We explored this issue using the supraoptic nucleus (SON) in lactating rats. At first, we identified the essential role of astrocytes in the milk-ejection reflex (MER) by disabling astrocytic functions via intracerebroventricular application of L-aminoadipic acid (L-AAA). L-AAA blocked the MER and reduced GFAP levels in the SON. In brain slices, L-AAA suppressed oxytocin (OT) neuronal activity and EPSCs. Suckling reduced GFAP in immunocytochemical images and in Western blots, reductions that were partially reversed after the MER. OT, the dominant hormone mediating the MER, reduced GFAP expression in brain slices. Tetanus toxin suppressed EPSCs but did not influence OT-reduced GFAP. Protease inhibitors did not influence OT-reduced GFAP images but blocked the degradation of GFAP molecules. In the presence of OT, transient 12 mM K⁺ exposure, simulating effects of synchronized bursts before the MER, reversed OT-reduced GFAP expression. Consistently, suckling first reduced and then increased the expression of aquaporin 4, astrocytic water channels coupled to K⁺ channels. Moreover, GFAP molecules were associated with astrocytic proteins, including aquaporin 4, actin, and glutamine synthetase and serine racemase. GFAP–aquaporin 4 association decreased during initial suckling and increased after the MER, whereas opposite changes occurred between GFAP and actin. MER also decreased the association between GFAP and glutamine synthetase. These results indicate that suckling elicits dynamic glial neuronal interactions in the SON; GFAP plasticity dynamically reflects OT neuronal activity.

Key words: excitability; Gfa (glial fibrillary acidic protein); imaging; lactation; protein; supraoptic

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Received Sept. 29, 2008; revised Nov. 21, 2008; accepted Dec. 19, 2008.

Correspondence should be addressed to Glenn I. Hatton, Department of Cell Biology and Neuroscience, University of California, Riverside, CA 92521. Email: glenn.hatton{at}ucr.edu

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