 |
||||
|
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, October 15, 1998, 18(20):8214-8227
Delayed Release of Neurotransmitter from Cerebellar Granule Cells
Pradeep P. Atluri and Wade G. Regehr Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115
At fast chemical synapses the rapid release of neurotransmitter that occurs within a few milliseconds of an action potential is followed by a more sustained elevation of release probability, known as delayed release. Here we characterize the role of calcium in delayed release and test the hypothesis that facilitation and delayed release share a common mechanism. Synapses between cerebellar granule cells and their postsynaptic targets, stellate cells and Purkinje cells, were studied in rat brain slices. Presynaptic calcium transients were measured with calcium-sensitive fluorophores, and delayed release was detected with whole-cell recordings. Calcium influx, presynaptic calcium dynamics, and the number of stimulus pulses were altered to assess their effect on delayed release and facilitation. Following single stimuli, delayed release can be separated into two components: one lasting for tens of milliseconds that is steeply calcium-dependent, the other lasting for hundreds of milliseconds that is driven by low levels of calcium with a nearly linear calcium dependence. The amplitude, calcium dependence, and magnitude of delayed release do not correspond to those of facilitation, indicating that these processes are not simple reflections of a shared mechanism. The steep calcium dependence of delayed release, combined with the large calcium transients observed in these presynaptic terminals, suggests that for physiological conditions delayed release provides a way for cells to influence their postsynaptic targets long after their own action potential activity has subsided.
Key words: delayed release; asynchronous release; calcium; stellate cell; granule cell; facilitation
Copyright © 1998 Society for Neuroscience 0270-6474/98/18208214-14$05.00/0
This article has been cited by other articles:
N. Strenzke, S. Chanda, C. Kopp-Scheinpflug, D. Khimich, K. Reim, A. V. Bulankina, A. Neef, F. Wolf, N. Brose, M. A. Xu-Friedman, et al.
Complexin-I Is Required for High-Fidelity Transmission at the Endbulb of Held Auditory Synapse
J. Neurosci., June 24, 2009; 29(25): 7991 - 8004.
[Abstract] [Full Text] [PDF]
K. J. Iremonger and J. S. Bains
Retrograde Opioid Signaling Regulates Glutamatergic Transmission in the Hypothalamus
J. Neurosci., June 3, 2009; 29(22): 7349 - 7358.
[Abstract] [Full Text] [PDF]
B. Rossi, G. Maton, and T. Collin
Calcium-permeable presynaptic AMPA receptors in cerebellar molecular layer interneurones
J. Physiol., November 1, 2008; 586(21): 5129 - 5145.
[Abstract] [Full Text] [PDF]
A. M. Kerr, E. Reisinger, and P. Jonas
Differential dependence of phasic transmitter release on synaptotagmin 1 at GABAergic and glutamatergic hippocampal synapses
PNAS, October 7, 2008; 105(40): 15581 - 15586.
[Abstract] [Full Text] [PDF]
X. Liu and C. Chen
Different Roles for AMPA and NMDA Receptors in Transmission at the Immature Retinogeniculate Synapse
J Neurophysiol, February 1, 2008; 99(2): 629 - 643.
[Abstract] [Full Text] [PDF]
S. D. Brenowitz and W. G. Regehr
Reliability and Heterogeneity of Calcium Signaling at Single Presynaptic Boutons of Cerebellar Granule Cells
J. Neurosci., July 25, 2007; 27(30): 7888 - 7898.
[Abstract] [Full Text] [PDF]
M. Xie, X. Li, J. Han, D. L. Vogt, S. Wittemann, M. D. Mark, and S. Herlitze
Facilitation versus depression in cultured hippocampal neurons determined by targeting of Ca2+ channel Cav{beta}4 versus Cav{beta}2 subunits to synaptic terminals
J. Cell Biol., July 24, 2007; 178(3): 489 - 502.
[Abstract] [Full Text] [PDF]
K. J. Iremonger and J. S. Bains
Integration of Asynchronously Released Quanta Prolongs the Postsynaptic Spike Window
J. Neurosci., June 20, 2007; 27(25): 6684 - 6691.
[Abstract] [Full Text] [PDF]
J. J. Crowley, A. G. Carter, and W. G. Regehr
Fast Vesicle Replenishment and Rapid Recovery from Desensitization at a Single Synaptic Release Site
J. Neurosci., May 16, 2007; 27(20): 5448 - 5460.
[Abstract] [Full Text] [PDF]
T. Sadakata, W. Kakegawa, A. Mizoguchi, M. Washida, R. Katoh-Semba, F. Shutoh, T. Okamoto, H. Nakashima, K. Kimura, M. Tanaka, et al.
Impaired Cerebellar Development and Function in Mice Lacking CAPS2, a Protein Involved in Neurotrophin Release
J. Neurosci., March 7, 2007; 27(10): 2472 - 2482.
[Abstract] [Full Text] [PDF]
F. Crepel
Developmental Changes in Retrograde Messengers Involved in Depolarization-Induced Suppression of Excitation at Parallel Fiber-Purkinje Cell Synapses in Rodents
J Neurophysiol, January 1, 2007; 97(1): 824 - 836.
[Abstract] [Full Text] [PDF]
Z. P. Pang, E. Melicoff, D. Padgett, Y. Liu, A. F. Teich, B. F. Dickey, W. Lin, R. Adachi, and T. C. Sudhof
Synaptotagmin-2 Is Essential for Survival and Contributes to Ca2+ Triggering of Neurotransmitter Release in Central and Neuromuscular Synapses
J. Neurosci., December 27, 2006; 26(52): 13493 - 13504.
[Abstract] [Full Text] [PDF]
T. Sakaba
Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of held.
J. Neurosci., May 31, 2006; 26(22): 5863 - 5871.
[Abstract] [Full Text] [PDF]
G. O. Hjelmstad
Interactions Between Asynchronous Release and Short-Term Plasticity in the Nucleus Accumbens Slice
J Neurophysiol, March 1, 2006; 95(3): 2020 - 2023.
[Abstract] [Full Text] [PDF]
J. I. Wadiche, A. V. Tzingounis, and C. E. Jahr
Intrinsic kinetics determine the time course of neuronal synaptic transporter currents
PNAS, January 24, 2006; 103(4): 1083 - 1087.
[Abstract] [Full Text] [PDF]
A. Warrier, S. Borges, D. Dalcino, C. Walters, and M. Wilson
Calcium From Internal Stores Triggers GABA Release From Retinal Amacrine Cells
J Neurophysiol, December 1, 2005; 94(6): 4196 - 4208.
[Abstract] [Full Text] [PDF]
K. Matsui, C. E. Jahr, and M. E. Rubio
High-Concentration Rapid Transients of Glutamate Mediate Neural-Glial Communication via Ectopic Release
J. Neurosci., August 17, 2005; 25(33): 7538 - 7547.
[Abstract] [Full Text] [PDF]
P.-M. Lau and G.-Q. Bi
Synaptic mechanisms of persistent reverberatory activity in neuronal networks
PNAS, July 19, 2005; 102(29): 10333 - 10338.
[Abstract] [Full Text] [PDF]
M. E. Calcagnotto and S. C. Baraban
Prolonged NMDA-Mediated Responses, Altered Ifenprodil Sensitivity, and Epileptiform-Like Events in the Malformed Hippocampus of Methylazoxymethanol Exposed Rats
J Neurophysiol, July 1, 2005; 94(1): 153 - 162.
[Abstract] [Full Text] [PDF]
C. Wyart, S. Cocco, L. Bourdieu, J.-F. Leger, C. Herr, and D. Chatenay
Dynamics of Excitatory Synaptic Components in Sustained Firing at Low Rates
J Neurophysiol, June 1, 2005; 93(6): 3370 - 3380.
[Abstract] [Full Text] [PDF]
E. Hui, J. Bai, P. Wang, M. Sugimori, R. R. Llinas, and E. R. Chapman
Three distinct kinetic groupings of the synaptotagmin family: Candidate sensors for rapid and delayed exocytosis
PNAS, April 5, 2005; 102(14): 5210 - 5214.
[Abstract] [Full Text] [PDF]
G. B. Awatramani, R. Turecek, and L. O. Trussell
Staggered Development of GABAergic and Glycinergic Transmission in the MNTB
J Neurophysiol, February 1, 2005; 93(2): 819 - 828.
[Abstract] [Full Text] [PDF]
T. Collin, M. Chat, M. G. Lucas, H. Moreno, P. Racay, B. Schwaller, A. Marty, and I. Llano
Developmental Changes in Parvalbumin Regulate Presynaptic Ca2+ Signaling
J. Neurosci., January 5, 2005; 25(1): 96 - 107.
[Abstract] [Full Text] [PDF]
D. P. Seeburg, X. Liu, and C. Chen
Frequency-Dependent Modulation of Retinogeniculate Transmission by Serotonin
J. Neurosci., December 1, 2004; 24(48): 10950 - 10962.
[Abstract] [Full Text] [PDF]
Y. Otsu and T. H. Murphy
Optical Postsynaptic Measurement of Vesicle Release Rates for Hippocampal Synapses Undergoing Asynchronous Release during Train Stimulation
J. Neurosci., October 13, 2004; 24(41): 9076 - 9086.
[Abstract] [Full Text] [PDF]
R. Lape and J. A. Dani
Complex Response to Afferent Excitatory Bursts by Nucleus Accumbens Medium Spiny Projection Neurons
J Neurophysiol, September 1, 2004; 92(3): 1276 - 1284.
[Abstract] [Full Text] [PDF]
A. Rancillac and F. Crepel
Synapses between parallel fibres and stellate cells express long-term changes in synaptic efficacy in rat cerebellum
J. Physiol., February 1, 2004; 554(3): 707 - 720.
[Abstract] [Full Text] [PDF]
Y. Otsu, V. Shahrezaei, B. Li, L. A. Raymond, K. R. Delaney, and T. H. Murphy
Competition between Phasic and Asynchronous Release for Recovered Synaptic Vesicles at Developing Hippocampal Autaptic Synapses
J. Neurosci., January 14, 2004; 24(2): 420 - 433.
[Abstract] [Full Text] [PDF]
M. Beierlein, J. R. Gibson, and B. W. Connors
Two Dynamically Distinct Inhibitory Networks in Layer 4 of the Neocortex
J Neurophysiol, November 1, 2003; 90(5): 2987 - 3000.
[Abstract] [Full Text] [PDF]
S. Kirischuk and R. Grantyn
Intraterminal Ca2+ concentration and asynchronous transmitter release at single GABAergic boutons in rat collicular cultures
J. Physiol., May 1, 2003; 548(3): 753 - 764.
[Abstract] [Full Text] [PDF]
A. R. Carter, C. Chen, P. M. Schwartz, and R. A. Segal
Brain-Derived Neurotrophic Factor Modulates Cerebellar Plasticity and Synaptic Ultrastructure
J. Neurosci., February 15, 2002; 22(4): 1316 - 1327.
[Abstract] [Full Text] [PDF]
A. G. Carter, K. E. Vogt, K. A. Foster, and W. G. Regehr
Assessing the Role of Calcium-Induced Calcium Release in Short-Term Presynaptic Plasticity at Excitatory Central Synapses
J. Neurosci., January 1, 2002; 22(1): 21 - 28.
[Abstract] [Full Text] [PDF]
E. Neher and T. Sakaba
Estimating Transmitter Release Rates from Postsynaptic Current Fluctuations
J. Neurosci., December 15, 2001; 21(24): 9638 - 9654.
[Abstract] [Full Text] [PDF]
S. Jacoby, R. E Sims, and N. A Hartell
Nitric oxide is required for the induction and heterosynaptic spread of long-term potentiation in rat cerebellar slices
J. Physiol., September 15, 2001; 535(3): 825 - 839.
[Abstract] [Full Text] [PDF]
Y. Li and R. E. Burke
Short-Term Synaptic Depression in the Neonatal Mouse Spinal Cord: Effects of Calcium and Temperature
J Neurophysiol, May 1, 2001; 85(5): 2047 - 2062.
[Abstract] [Full Text] [PDF]
M. A. Xu-Friedman and W. G. Regehr
Probing Fundamental Aspects of Synaptic Transmission with Strontium
J. Neurosci., June 15, 2000; 20(12): 4414 - 4422.
[Abstract] [Full Text] [PDF]
A. G. Carter and W. G. Regehr
Prolonged Synaptic Currents and Glutamate Spillover at the Parallel Fiber to Stellate Cell Synapse
J. Neurosci., June 15, 2000; 20(12): 4423 - 4434.
[Abstract] [Full Text] [PDF]
S. B. Kombian, M. Hirasawa, D. Mouginot, X. Chen, and Q. J. Pittman
Short-Term Potentiation of Miniature Excitatory Synaptic Currents Causes Excitation of Supraoptic Neurons
J Neurophysiol, May 1, 2000; 83(5): 2542 - 2553.
[Abstract] [Full Text] [PDF]
A. C. Kreitzer and W. G. Regehr
Modulation of Transmission during Trains at a Cerebellar Synapse
J. Neurosci., February 15, 2000; 20(4): 1348 - 1357.
[Abstract] [Full Text] [PDF]
C. Chen and W. G. Regehr
Contributions of Residual Calcium to Fast Synaptic Transmission
J. Neurosci., August 1, 1999; 19(15): 6257 - 6266.
[Abstract] [Full Text] [PDF]
T. Karhunen, F. S. Vilim, V. Alexeeva, K. R. Weiss, and P. J. Church
Targeting of Peptidergic Vesicles in Cotransmitting Terminals
J. Neurosci., February 1, 2001; 21(3): RC127 - RC127.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|