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The Journal of Neuroscience, February 11, 2004, 24(6):1358-1365; doi:10.1523/JNEUROSCI.4022-03.2004

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Cellular/Molecular
Diversity of Functional Astroglial Properties in the Respiratory Network

Dennis Graß,¹ Petra G. Pawlowski,^2 * Johannes Hirrlinger,^2,3 * Nestoras Papadopoulos,¹ Diethelm W. Richter,¹ Frank Kirchhoff,² and Swen Hülsmann¹

¹Department of Neuro- and Sensory Physiology, Center for Physiology and Pathophysiology, Georg-August-University, 37073 Göttingen, Germany, ²Department of Neurogenetics, Max Planck Institute of Experimental Medicine, 37075 Göttingen, Germany, and ³DFG-Research Center for Molecular Physiology of the Brain, 37073 Göttingen, Germany

A population of neurons in the caudal medulla generates the rhythmic activity underlying breathing movements. Although this neuronal network has attracted great attention for studying neuronal aspects of synaptic transmission, functions of glial cells supporting this neuronal activity remain unclear. To investigate the role of astrocytes in the respiratory network, we applied electrophysiological and immunohistochemical techniques to characterize astrocytes in regions involved in the generation and transmission of rhythmic activity. In the ventral respiratory group and the hypoglossal nucleus (XII) of acutely isolated brainstem slices, we analyzed fluorescently labeled astrocytes obtained from TgN(GFAP-EGFP) transgenic mice with the whole-cell voltage-clamp technique. Three subpopulations of astrocytes could be discerned by their distinct membrane current profiles. A first group of astrocytes was characterized by nonrectifying, symmetrical and voltage-independent potassium currents and a robust glutamate transporter response to D-aspartate. A second group of astrocytes showed additional A-type potassium currents, whereas a third group, identified by immunolabeling for the glial progenitor marker NG2, expressed outwardly rectifying potassium currents, smaller potassium inward currents, and only minimal D-aspartate-induced transporter currents. Astrocytes of all groups showed kainate-induced inward currents.

We conclude that most of the astrocytes serve as a buffer system of excess extracellular glutamate and potassium; however, a distinct cell population (NG2-positive, A-type potassium currents) may play an important role for network plasticity.

Key words: brainstem; GFAP (glial fibrillary acidic protein); EGFP; glutamate; potassium (K); neuron-glia interaction

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Received Sep 1, 2003; revised November 28, 2003; accepted December 9, 2003.

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