Putative Single Quantum and Single Fibre Excitatory Postsynaptic Currents Show Similar Amplitude Range and Variability in Rat Hippocampal Slices

Transmission at excitatory synapses in the mammalian brain is thought to depend on the release of transmitter quanta through exocytosis of presynaptic vesicles (Katz, 1969). The number of vesicles released by a single presynaptic action potential is important for understanding the impact of a single synapse, and the variability in transmission from one impulse to the next. In addition, the number of vesicles released may be an important factor for synaptic regulation and plasticity, such as facilitation, post‐tetanic potentiation and long‐term potentiation (LTP). Three recent studies suggest that an increase in the number of transmitter quanta underlies hippocampal LTP (Malinow and Tsien, 1990; Bekkers and Stevens 1990; Malinow, 1991), whereas other reports suggest a postsynaptic mechanism (Kauer et al 1988; Muller et al, 1988; Foster and McNaughton, 1989). We have used the whole‐cell recording technique to compare putative quantal and single fibre responses at excitatory synapses in rat hippocampal slices, and find (i) a surprisingly large variability in single fibre excitatory postsynaptic currents (sfEPSCs); (ii) an equally large variability of putative quantal (pq) EPSCs elicited by hyperosmolar media or ruthenium red; (iii) the observed amplitude ranges for the sfEPSCs and the pqEPSCs overlap almost completely; and (iv) in neither case can the variability be attributed to a scatter in electrotonic distance from the soma of the engaged synapses. Thus, the data are compatible with the hypothesis that a presynaptic action potential usually releases only a single quantum. Other possibilities are also discussed.

[1]  B. Katz,et al.  Spontaneous subthreshold activity at motor nerve endings , 1952, The Journal of physiology.

[2]  W. Rall Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. , 1967, Journal of neurophysiology.

[3]  E. Alnaes,et al.  On the role of mitochondria in transmitter release from motor nerve terminals. , 1975, The Journal of physiology.

[4]  J. Jack,et al.  The components of synaptic potentials evoked in cat spinal motoneurones by impulses in single group Ia afferents. , 1981, The Journal of physiology.

[5]  G. Lynch,et al.  Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. , 1988, Science.

[6]  R. Nicoll,et al.  A persistent postsynaptic modification mediates long-term potentiation in the hippocampus , 1988, Neuron.

[7]  C. Stevens,et al.  NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus , 1989, Nature.

[8]  P. Andersen,et al.  Amplitude fluctuations in small EPSPs recorded from CA1 pyramidal cells in the guinea pig hippocampal slice , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Arnold R. Kriegstein,et al.  Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex , 1989, Journal of Neuroscience Methods.

[10]  C. Stevens,et al.  Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[11]  M. Jackson,et al.  Miniature excitatory synaptic currents in cultured hippocampal neurons , 1990, Brain Research.

[12]  B Sakmann,et al.  Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch‐clamp study. , 1990, The Journal of physiology.

[13]  C. Stevens,et al.  Presynaptic mechanism for long-term potentiation in the hippocampus , 1990, Nature.

[14]  M. J. Friedlander,et al.  Evaluation of long-term potentiation of small compound and unitary EPSPs at the hippocampal CA3-CA1 synapse , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  R. Tsien,et al.  Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices , 1990, Nature.

[16]  K. Stratford,et al.  Quantal analysis of excitatory synaptic action and depression in hippocampal slices , 1991, Nature.

[17]  R. Malinow Transmission between pairs of hippocampal slice neurons: quantal levels, oscillations, and LTP. , 1991, Science.

[18]  W. G. Van der Kloot The regulation of quantal size. , 1997, Progress in neurobiology.