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The Journal of Neuroscience, January 10, 2007, 27(2):341-354; doi:10.1523/JNEUROSCI.4051-06.2007

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Cellular/Molecular
Fast Synaptic Vesicle Reuse Slows the Rate of Synaptic Depression in the CA1 Region of Hippocampus

Mert Ertunc, Yildirim Sara, ChiHye Chung, Deniz Atasoy, Tuhin Virmani, and Ege T. Kavalali

Center for Basic Neuroscience and Department of Physiology, The University of Texas Southwestern Medical Center, Dallas, Texas 75390-9111

Correspondence should be addressed to Dr. Ege T. Kavalali, Center for Basic Neuroscience, The University of Texas, Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9111. Email: Ege.Kavalali{at}UTSouthwestern.edu

During short-term synaptic depression, neurotransmission rapidly decreases in response to repetitive action potential firing. Here, by blocking the vacuolar ATPase, alkalinizing the extracellular pH, or exposing hippocampal slices to pH buffers, we impaired neurotransmitter refilling, and electrophysiologically tested the role of vesicle reuse in synaptic depression. Under all conditions, synapses onto hippocampal CA1 pyramidal cells showed faster depression with increasing stimulation frequencies. At 20 Hz, compromising neurotransmitter refilling increased depression within 300 ms reaching completion within 2 s, suggesting a minimal contribution of reserve vesicles to neurotransmission. In contrast, at 1 Hz, depression emerged gradually and became significant within 100 s. Moreover, the depression induced by pH buffers was reversible with a similar frequency dependence, suggesting that the frequency-dependent increase in depression was caused by impairment of rapid synaptic vesicle reuse. These results indicate that synaptic vesicle trafficking impacts the kinetics of short-term synaptic plasticity at an extremely rapid time scale.

Key words: synaptic vesicle recycling; hippocampal slice; short term synaptic depression; vesicle reacidification; endocytosis; CA1; Schaffer collateral

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Received April 13, 2006; revised Dec. 4, 2006; accepted Dec. 5, 2006.

Correspondence should be addressed to Dr. Ege T. Kavalali, Center for Basic Neuroscience, The University of Texas, Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9111. Email: Ege.Kavalali{at}UTSouthwestern.edu

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