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The Journal of Neuroscience, January 16, 2008, 28(3):725-731; doi:10.1523/JNEUROSCI.3625-07.2008

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Cellular/Molecular
Kainate Modulates Presynaptic GABA Release from Two Vesicle Pools

Seena S. Mathew, Lucas Pozzo-Miller, and John J. Hablitz

Department of Neurobiology and Evelyn F. McKnight Brain Institute, University of Alabama at Birmingham, Birmingham, Alabama 35294

Correspondence should be addressed to Dr. John J. Hablitz, Department of Neurobiology, University of Alabama at Birmingham, Birmingham, AL 35294. Email: jhablitz{at}uab.edu

Inhibitory control of local neuronal circuits is critical for prefrontal cortical functioning. Modulation of inhibitory circuits by several neuromodulators has been demonstrated, but the underlying mechanisms are unclear. Neuromodulator effects on synaptic vesicle recycling have received little attention. Controversy also exists whether different pools of synaptic vesicles underlie spontaneous and activity-dependent vesicle recycling. We therefore investigated the effects of kainate receptor activation on GABA release in rat prefrontal neocortex using electrophysiological and styryl dye imaging techniques in acute neocortical slices. Electrophysiological studies demonstrated that activation of kainate receptors increased the frequency, but not the amplitude of miniature IPSCs, suggesting a presynaptic action. Using styryl dye staining and multiphoton excitation microscopy, we visualized vesicular release from inhibitory GABAergic terminals in prefrontal cortical slices and demonstrate that kainate facilitates GABA release from presynaptic terminals. Our findings also indicate the presence of two pools of GABA-containing vesicles within inhibitory terminals. Kainate modulates both pools but only when vesicles are endocytosed and exocytosed by matching protocols of dye loading, i.e., spontaneous or evoked afferent activity.

Key words: neocortex; kainate; GABA; vesicular release; FM1-43; inhibition; multiphoton excitation microscopy; brain slices

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Received Aug. 9, 2007; revised Nov. 16, 2007; accepted Dec. 3, 2007.

Correspondence should be addressed to Dr. John J. Hablitz, Department of Neurobiology, University of Alabama at Birmingham, Birmingham, AL 35294. Email: jhablitz{at}uab.edu

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