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The Journal of Neuroscience, September 12, 2007, 27(37):9846-9854; doi:10.1523/JNEUROSCI.2803-07.2007

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Cellular/Molecular
Vesicle Pool Heterogeneity at Hippocampal Glutamate and GABA Synapses

Krista L. Moulder,¹ Xiaoping Jiang,¹ Amanda A. Taylor,¹ Wonchul Shin,^3,5 Kevin D. Gillis,^3,4,5 and Steven Mennerick^1,2

Departments of ¹Psychiatry and ²Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110, and Departments of ³Biological Engineering and ⁴Medical Pharmacology and Physiology and the ⁵Dalton Cardiovascular Research Center, University of Missouri–Columbia Research Park, Columbia, Missouri 65211

Correspondence should be addressed to Dr. Krista Moulder, Department of Psychiatry, Washington University School of Medicine, 660 South Euclid Avenue, Box 8134, St. Louis, MO 63110. Email: moulderk{at}psychiatry.wustl.edu

Glutamate and GABA are the major fast excitatory and inhibitory neurotransmitters, respectively, in the CNS. Although glutamate and GABA have clearly distinct postsynaptic actions, we are just beginning to appreciate that presynaptic differences between glutamatergic and GABAergic neurons may contribute to distinct functions of these transmitter systems. We therefore probed possible differences between the functional synaptic vesicle populations of glutamatergic and GABAergic neurons. We examined superecliptic synaptopHluorin (SpH) fluorescence during 20 Hz electrical stimulation in transfected hippocampal neurons and identified the phenotype of SpH-fluorescent synapses with post hoc immunostaining. With 200 stimuli (10 s), individual glutamate synapses displayed considerably more variability in peak SpH fluorescence than GABA synapses, without a strong difference in the mean SpH fluorescence increase. This spatial heterogeneity could not be accounted for by differences in endocytosis, which was nearly constant over these short time periods across glutamate and GABA synapses. Instead, variability in vesicle exocytosis correlated with variability in total vesicle staining and in measures of the total recycling pool size. Differences were also evident using FM1-43 [N-(3-triethylammoniumpropyl)-4-(4-(dibutylamino)styryl) pyridinium dibromide] uptake. These data support the idea that the population of glutamate synapses exhibits more heterogeneity in release properties than the population of GABA synapses, possibly correlated with glutamatergic synaptic malleability.

Key words: synaptopHluorin; exocytosis; endocytosis; recycling pool; synaptic strength; transfection

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Received March 16, 2007; revised July 18, 2007; accepted July 21, 2007.

Correspondence should be addressed to Dr. Krista Moulder, Department of Psychiatry, Washington University School of Medicine, 660 South Euclid Avenue, Box 8134, St. Louis, MO 63110. Email: moulderk{at}psychiatry.wustl.edu

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