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The Journal of Neuroscience, February 1, 2006, 26(5):1366-1377; doi:10.1523/JNEUROSCI.3889-05.2006

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Cellular/Molecular
Physiological Temperatures Reduce the Rate of Vesicle Pool Depletion and Short-Term Depression via an Acceleration of Vesicle Recruitment

Christopher Kushmerick,^1 * Robert Renden,^2 * and Henrique von Gersdorff²

¹Departamento de Fisiologia e Biofísica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, 31270-901 Minas Gerais, Brasil, and ²The Vollum Institute, Oregon Health and Science University, Portland, Oregon 97239

Correspondence should be addressed to Henrique von Gersdorff, The Vollum Institute, Oregon Health and Science University, 3181 Southwest Sam Jackson Park Road, Portland, OR 97239-3098. Email: vongersd{at}ohsu.edu

The timing and strength of synaptic transmission is profoundly dependent on temperature. However, the temperature dependence of the multiple mechanisms that contribute to short-term synaptic plasticity is poorly understood. Here, we use voltage-clamp recordings to quantify the temperature dependence of exocytosis at the calyx of Held synapse. EPSC and miniature EPSC amplitudes were larger at physiological temperature, but quantal content during low-frequency (0.05 Hz) stimulation was constant after temperature jumps from 22–24°C to 35–37°C. The initial degree of EPSC depression during 100 Hz stimuli trains was unchanged with temperature, as were estimates of release probability and vesicle pool size. In contrast, physiological temperatures dramatically relieved depression measured after 40 stimuli at 100 Hz by increasing twofold the rate of recovery from depression. Presynaptic calyx recordings revealed that physiological temperature increased capacitance jumps resulting from 0.5 and 1 ms depolarizations by increasing Ca²⁺ influx. When Ca²⁺ entry was equalized at the two temperatures, exocytosis exhibited little temperature dependence for brief depolarizations. However, in response to longer depolarizations, raising temperature increased a slow phase of exocytosis, without affecting overall Ca²⁺ entry or the size of the readily releasable pool of vesicles. Higher temperatures also increased the rate of presynaptic Ca²⁺ current inactivation; nevertheless, the degree of steady-state EPSC depression was greatly reduced. Our results thus suggest that changes in steady-state EPSCs during stimulus trains at physiological temperature reflect larger quantal amplitudes and faster refilling of synaptic vesicle pools, leading to reduced short-term depression during prolonged high-frequency firing.

Key words: auditory brainstem; development; calyx of Held; MNTB; exocytosis; glutamate release; short-term synaptic plasticity; AMPA receptor desensitization; presynaptic Ca²⁺ current

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Received Sept. 14, 2005; revised Dec. 6, 2005; accepted Dec. 12, 2005.

Correspondence should be addressed to Henrique von Gersdorff, The Vollum Institute, Oregon Health and Science University, 3181 Southwest Sam Jackson Park Road, Portland, OR 97239-3098. Email: vongersd{at}ohsu.edu

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