Abstract
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.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 1366-1377 |
| Number of pages | 12 |
| Journal | Journal of Neuroscience |
| Volume | 26 |
| Issue number | 5 |
| DOIs | |
| State | Published - Feb 1 2006 |
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Keywords
- AMPA receptor desensitization
- Auditory brainstem
- Calyx of Held
- Development
- Exocytosis
- Glutamate release
- MNTB
- Presynaptic Ca current
- Short-term synaptic plasticity
ASJC Scopus subject areas
- Neuroscience(all)
Cite this
Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. / Kushmerick, Christopher; Renden, Robert; Von Gersdorff, Henrique.
In: Journal of Neuroscience, Vol. 26, No. 5, 01.02.2006, p. 1366-1377.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment
AU - Kushmerick, Christopher
AU - Renden, Robert
AU - Von Gersdorff, Henrique
PY - 2006/2/1
Y1 - 2006/2/1
N2 - 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.
AB - 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.
KW - AMPA receptor desensitization
KW - Auditory brainstem
KW - Calyx of Held
KW - Development
KW - Exocytosis
KW - Glutamate release
KW - MNTB
KW - Presynaptic Ca current
KW - Short-term synaptic plasticity
UR - http://www.scopus.com/inward/record.url?scp=32544434225&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=32544434225&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.3889-05.2006
DO - 10.1523/JNEUROSCI.3889-05.2006
M3 - Article
C2 - 16452660
AN - SCOPUS:32544434225
VL - 26
SP - 1366
EP - 1377
JO - Journal of Neuroscience
JF - Journal of Neuroscience
SN - 0270-6474
IS - 5
ER -