Effective release rates at single rat Schaffer collateral-CA1 synapses during sustained theta-burst activity revealed by optical imaging
- 5 July 2007
- journal article
- Published by Wiley in The Journal of Physiology
- Vol. 582 (2), 583-595
- https://doi.org/10.1113/jphysiol.2007.130286
Abstract
To understand how information is coded at single hippocampal synapses during high-frequency activity, we imaged NMDA receptor-mediated Ca(2+) responses in spines of CA1 neurons using two-photon microscopy. Although discrete quantal events were not readily apparent during continuous theta-burst stimulation (TBS), we found that the steady-state dendritic Ca(2+) response was spatially restricted (half-width < 1 microm), voltage dependent and sensitive to MK-801, indicating that that it was mediated by activation of NMDA receptors at single synapses. Partial antagonism of NMDA receptors caused a similar reduction of NMDA EPSCs (measured at the soma) and local dendritic Ca(2+) signals, suggesting that, like EPSCs, the steady-state Ca(2+) signal was made up of a linear addition of quantal events. Statistical analyses of the steady-response suggested that the quantal size did not change dramatically during TBS. Deconvolution of TBS-evoked Ca(2+) responses revealed a heterogeneous population of synapses differing in their capacity to signal high-frequency information, with an average effective steady-state release rate of approximately 2.6 vesicles synapse(-1)s(-1). To assess how the optically determined release rates compare with population measures we analysed the rate of decay of peak EPSCs during train stimulation. From these studies, we estimated a unitary vesicular replenishment rate of 0.02 s(-1), which corresponds to an average release rate of approximately 0.8-2 vesicles s(-1) at individual synapses. Additionally, extracellular recordings from single Schaffer collaterals revealed that spikes propagate reliably during TBS. Hence, during high-frequency activity, Schaffer collaterals conduct spikes with high fidelity, but release quanta with relatively lower efficiency, leaving NMDA receptor function largely intact and synapse specific. Heterogeneity in release rates between synapses suggests that similar patterns of presynaptic action potentials could trigger different forms of plasticity at individual synapses.This publication has 71 references indexed in Scilit:
- Clathrin-Mediated Endocytosis Is the Dominant Mechanism of Vesicle Retrieval at Hippocampal SynapsesNeuron, 2006
- BDNF increases release probability and the size of a rapidly recycling vesicle pool within rat hippocampal excitatory synapsesThe Journal of Physiology, 2006
- Frequency-Dependent Kinetics and Prevalence of Kiss-and-Run and Reuse at Hippocampal Synapses Studied with Novel Quenching MethodsNeuron, 2006
- Synaptic vesicle poolsNature Reviews Neuroscience, 2005
- Competition between Phasic and Asynchronous Release for Recovered Synaptic Vesicles at Developing Hippocampal Autaptic SynapsesJournal of Neuroscience, 2004
- The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neuronsThe Journal of Physiology, 2002
- Enhancement of presynaptic calcium current by cysteine string proteinThe Journal of Physiology, 2002
- Saturation of postsynaptic receptors at central synapses?Current Opinion in Neurobiology, 1996
- Visualization of Quantal Synaptic Transmission by Dendritic Calcium ImagingScience, 1994
- EVIDENCE FOR RECYCLING OF SYNAPTIC VESICLE MEMBRANE DURING TRANSMITTER RELEASE AT THE FROG NEUROMUSCULAR JUNCTIONThe Journal of cell biology, 1973