 |
Previous Article | Next Article 
Volume 17, Number 10,
Issue of May 15, 1997
pp. 3425-3435
Copyright ©1997 Society for Neuroscience
Control of Neurotransmitter Release by Presynaptic Waveform at
the Granule Cell to Purkinje Cell Synapse
Received Jan. 24, 1997; revised Feb. 25, 1997; accepted Feb. 26, 1997.
Bernardo L. Sabatini and
Wade G. Regehr
Department of Neurobiology, Harvard Medical School, Boston,
Massachusetts 02115
The effect of changes in the shape of the presynaptic action
potential on neurotransmission was examined at synapses between granule
and Purkinje cells in slices from the rat cerebellum. Low
concentrations of tetraethylammonium were used to broaden the
presynaptic action potential. The presynaptic waveform was monitored
with voltage-sensitive dyes, the time course and amplitude of
presynaptic calcium entry were determined with fluorescent calcium
indicators, and EPSCs were measured with a whole-cell voltage clamp.
Spike broadening increased calcium influx primarily by prolonging
calcium entry without greatly affecting peak presynaptic calcium
currents, indicating that the majority of calcium channels reach
maximal probability of opening in response to a single action potential
and that spike broadening increases the open time of these channels.
EPSCs were exquisitely sensitive to elevations of calcium influx
produced by spike broadening; there was a high power relationship
between calcium influx and release such that a 23% increase in spike
width led to a 25% increase in total calcium influx, which in turn
doubled synaptic strength.
The finding that even small changes in spike width influence
neurotransmitter release suggests that altering the presynaptic waveform may be an important means of modifying the strength of this
synapse. Waveform changes do not, however, contribute significantly to
presynaptic modulation via activation of adenosine A1 or
GABAB receptors. Furthermore, greatly reducing presynaptic
calcium influx did not alter the presynaptic waveform, indicating that
calcium channels and calcium-activated channels do not participate in shaping the presynaptic waveform.
Key words:
synaptic transmission;
spike broadening;
parallel fiber;
Purkinje cell;
tetraethylammonium;
voltage-sensitive dyes;
calcium-sensitive indicators.
This article has been cited by other articles:

|
 |

|
 |
 
P. Lirk, M. Poroli, M. Rigaud, A. Fuchs, P. Fillip, C.-Y. Huang, M. Ljubkovic, D. Sapunar, and Q. Hogan
Modulators of Calcium Influx Regulate Membrane Excitability in Rat Dorsal Root Ganglion Neurons
Anesth. Analg.,
August 1, 2008;
107(2):
673 - 685.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. M. Sonner, J. A. Filosa, and J. E. Stern
Diminished A-type potassium current and altered firing properties in presympathetic PVN neurones in renovascular hypertensive rats
J. Physiol.,
March 15, 2008;
586(6):
1605 - 1622.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Gundlfinger, J. Bischofberger, F. W. Johenning, M. Torvinen, D. Schmitz, and J. Breustedt
Adenosine modulates transmission at the hippocampal mossy fibre synapse via direct inhibition of presynaptic calcium channels
J. Physiol.,
July 1, 2007;
582(1):
263 - 277.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Fedchyshyn and L.-Y. Wang
Activity-dependent changes in temporal components of neurotransmission at the juvenile mouse calyx of Held synapse
J. Physiol.,
June 1, 2007;
581(2):
581 - 602.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Chaudhuri, J. B. Issa, and D. T. Yue
Elementary Mechanisms Producing Facilitation of Cav2.1 (P/Q-type) Channels
J. Gen. Physiol.,
April 30, 2007;
129(5):
385 - 401.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. A. Rusakov
Ca2+-Dependent Mechanisms of Presynaptic Control at Central Synapses
Neuroscientist,
August 1, 2006;
12(4):
317 - 326.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-M. Yang and L.-Y. Wang
Amplitude and Kinetics of Action Potential-Evoked Ca2+ Current and Its Efficacy in Triggering Transmitter Release at the Developing Calyx of Held Synapse
J. Neurosci.,
May 24, 2006;
26(21):
5698 - 5708.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-J. Jeng, Y.-T. Chen, Y.-W. Chen, and C.-Y. Tang
Dominant-negative effects of human P/Q-type Ca2+ channel mutations associated with episodic ataxia type 2
Am J Physiol Cell Physiol,
April 1, 2006;
290(4):
C1209 - C1220.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Khavandgar, J. T. Walter, K. Sageser, and K. Khodakhah
Kv1 channels selectively prevent dendritic hyperexcitability in rat Purkinje cells
J. Physiol.,
December 1, 2005;
569(2):
545 - 557.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. P Meeks, X. Jiang, and S. Mennerick
Action potential fidelity during normal and epileptiform activity in paired soma-axon recordings from rat hippocampus
J. Physiol.,
July 15, 2005;
566(2):
425 - 441.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. G. de Polavieja, A. Harsch, I. Kleppe, H. P. C. Robinson, and M. Juusola
Stimulus History Reliably Shapes Action Potential Waveforms of Cortical Neurons
J. Neurosci.,
June 8, 2005;
25(23):
5657 - 5665.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Mutoh, Q. Yuan, and T. Knopfel
Long-Term Depression at Olfactory Nerve Synapses
J. Neurosci.,
April 27, 2005;
25(17):
4252 - 4259.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Fedchyshyn and L.-Y. Wang
Developmental Transformation of the Release Modality at the Calyx of Held Synapse
J. Neurosci.,
April 20, 2005;
25(16):
4131 - 4140.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. J Stephens and S. Mochida
G protein {beta}{gamma} subunits mediate presynaptic inhibition of transmitter release from rat superior cervical ganglion neurones in culture
J. Physiol.,
March 15, 2005;
563(3):
765 - 776.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. G. Inchauspe, F. J. Martini, I. D. Forsythe, and O. D. Uchitel
Functional Compensation of P/Q by N-Type Channels Blocks Short-Term Plasticity at the Calyx of Held Presynaptic Terminal
J. Neurosci.,
November 17, 2004;
24(46):
10379 - 10383.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Beierlein, K. R. Gee, V. V. Martin, and W. G. Regehr
Presynaptic Calcium Measurements at Physiological Temperatures Using a New Class of Dextran-Conjugated Indicators
J Neurophysiol,
July 1, 2004;
92(1):
591 - 599.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. P. Brown, P. K. Safo, and W. G. Regehr
Endocannabinoids Inhibit Transmission at Granule Cell to Purkinje Cell Synapses by Modulating Three Types of Presynaptic Calcium Channels
J. Neurosci.,
June 16, 2004;
24(24):
5623 - 5631.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Raffaelli, C. Saviane, M. H. Mohajerani, P. Pedarzani, and E. Cherubini
BK potassium channels control transmitter release at CA3-CA3 synapses in the rat hippocampus
J. Physiol.,
May 15, 2004;
557(1):
147 - 157.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Isope, R. Franconville, B. Barbour, and P. Ascher
Repetitive firing of rat cerebellar parallel fibres after a single stimulation
J. Physiol.,
February 1, 2004;
554(3):
829 - 839.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. E. Niven and M. Burrows
Spike Width Reduction Modifies the Dynamics of Short-Term Depression at a Central Synapse in the Locust
J. Neurosci.,
August 20, 2003;
23(20):
7461 - 7469.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Matsukawa, A. M. Wolf, S. Matsushita, R. H. Joho, and T. Knopfel
Motor Dysfunction and Altered Synaptic Transmission at the Parallel Fiber-Purkinje Cell Synapse in Mice Lacking Potassium Channels Kv3.1 and Kv3.3
J. Neurosci.,
August 20, 2003;
23(20):
7677 - 7684.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Juusola and G. G. de Polavieja
The Rate of Information Transfer of Naturalistic Stimulation by Graded Potentials
J. Gen. Physiol.,
July 28, 2003;
122(2):
191 - 206.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. D. Brenowitz and W. G. Regehr
Calcium Dependence of Retrograde Inhibition by Endocannabinoids at Synapses onto Purkinje Cells
J. Neurosci.,
July 16, 2003;
23(15):
6373 - 6384.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Bischofberger, J. R. P. Geiger, and P. Jonas
Timing and Efficacy of Ca2+ Channel Activation in Hippocampal Mossy Fiber Boutons
J. Neurosci.,
December 15, 2002;
22(24):
10593 - 10602.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Kamiya, S. Ozawa, and T. Manabe
Kainate Receptor-Dependent Short-Term Plasticity of Presynaptic Ca2+ Influx at the Hippocampal Mossy Fiber Synapses
J. Neurosci.,
November 1, 2002;
22(21):
9237 - 9243.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Lowe
Inhibition of Backpropagating Action Potentials in Mitral Cell Secondary Dendrites
J Neurophysiol,
July 1, 2002;
88(1):
64 - 85.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Bertram, M. I. Arnot, and G. W. Zamponi
Role for G Protein Gbeta gamma Isoform Specificity in Synaptic Signal Processing: A Computational Study
J Neurophysiol,
May 1, 2002;
87(5):
2612 - 2623.
[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]
|
 |
|

|
 |

|
 |
 
Y. He, C. F. Zorumski, and S. Mennerick
Contribution of Presynaptic Na+ Channel Inactivation to Paired-Pulse Synaptic Depression in Cultured Hippocampal Neurons
J Neurophysiol,
February 1, 2002;
87(2):
925 - 936.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Espinosa, A. McMahon, E. Chan, S. Wang, C. S. Ho, N. Heintz, and R. H. Joho
Alcohol Hypersensitivity, Increased Locomotion, and Spontaneous Myoclonus in Mice Lacking the Potassium Channels Kv3.1 and Kv3.3
J. Neurosci.,
September 1, 2001;
21(17):
6657 - 6665.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. E. Stewart and R. C. Foehring
Effects of Spike Parameters and Neuromodulators on Action Potential Waveform-Induced Calcium Entry Into Pyramidal Neurons
J Neurophysiol,
April 1, 2001;
85(4):
1412 - 1423.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. M. Colecraft, D. L. Brody, and D. T. Yue
G-Protein Inhibition of N- and P/Q-Type Calcium Channels: Distinctive Elementary Mechanisms and Their Functional Impact
J. Neurosci.,
February 15, 2001;
21(4):
1137 - 1147.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. S. Livingston and R. Mooney
Androgens and Isolation From Adult Tutors Differentially Affect the Development of Songbird Neurons Critical to Vocal Plasticity
J Neurophysiol,
January 1, 2001;
85(1):
34 - 42.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Taschenberger and H. von Gersdorff
Fine-Tuning an Auditory Synapse for Speed and Fidelity: Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and Synaptic Plasticity
J. Neurosci.,
December 15, 2000;
20(24):
9162 - 9173.
[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]
|
 |
|

|
 |

|
 |
 
C. C. Gandhi and L. D. Matzel
Modulation of Presynaptic Action Potential Kinetics Underlies Synaptic Facilitation of Type B Photoreceptors after Associative Conditioning in Hermissenda
J. Neurosci.,
March 1, 2000;
20(5):
2022 - 2035.
[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]
|
 |
|

|
 |

|
 |
 
R. H. Joho, C. S. Ho, and G. A. Marks
Increased gamma - and Decreased delta -Oscillations in a Mouse Deficient for a Potassium Channel Expressed in Fast-Spiking Interneurons
J Neurophysiol,
October 1, 1999;
82(4):
1855 - 1864.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Msghina, A. G. Millar, M. P. Charlton, C. K. Govind, and H. L. Atwood
Calcium Entry Related to Active Zones and Differences in Transmitter Release at Phasic and Tonic Synapses
J. Neurosci.,
October 1, 1999;
19(19):
8419 - 8434.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R.-L. Wu and M. E. Barish
Modulation of a Slowly Inactivating Potassium Current, ID, by Metabotropic Glutamate Receptor Activation in Cultured Hippocampal Pyramidal Neurons
J. Neurosci.,
August 15, 1999;
19(16):
6825 - 6837.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Qian and P. Saggau
Modulation of Transmitter Release by Action Potential Duration at the Hippocampal CA3-CA1 Synapse
J Neurophysiol,
January 1, 1999;
81(1):
288 - 298.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. D. Whim and L. K. Kaczmarek
Heterologous Expression of the Kv3.1 Potassium Channel Eliminates Spike Broadening and the Induction of a Depolarizing Afterpotential in the Peptidergic Bag Cell Neurons
J. Neurosci.,
November 15, 1998;
18(22):
9171 - 9180.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Takahashi, Y. Kajikawa, and T. Tsujimoto
G-Protein-Coupled Modulation of Presynaptic Calcium Currents and Transmitter Release by a GABAB Receptor
J. Neurosci.,
May 1, 1998;
18(9):
3138 - 3146.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Chen and W. G. Regehr
The Mechanism of cAMP-Mediated Enhancement at a Cerebellar Synapse
J. Neurosci.,
November 15, 1997;
17(22):
8687 - 8694.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|