Quantal properties of spontaneous EPSCs in neurones of the guinea‐pig dorsal lateral geniculate nucleus.

1. Spontaneous non‐NMDA glutamate receptor‐mediated EPSCs were recorded with the whole‐cell patch‐clamp technique from twenty‐six neurones in the dorsal lateral geniculate nucleus in thalamic slices from guinea‐pig. 2. Amplitude distributions of the EPSCs were skewed towards larger values. The skewness could be accounted for by multiquantal properties. The multiquantal properties were most clearly demonstrated in four cells that had prominent peaks in the amplitude distribution, and peak separation approximately corresponding to the modal value. The amplitude distribution for all cells could be adequately fitted by a quantal model consisting of a sum of Gaussians with means equal to integer multiples of a quantal unit. The variance of each Gaussian was equal to the sum of the noise variance of the recordings and an additional non‐negative variance which increased linearly with the number of the Gaussian in the series. The estimated mean quantal size was 152 +/‐ 37 pS. The estimated mean quantal coefficient of variation was 15%. Addition of tetrodotoxin did not significantly change any of the quantal parameters (n = 5). 3. The waveform of the EPSCs was similar for small and large events, and similar to that of events evoked by stimulation of retinal input fibres. There was a positive correlation between peak amplitude and rise time. This is the opposite of that expected if differences in electrotonic distances were to explain differences in amplitude. 4. The spontaneous EPSCs occurred randomly at an average frequency of 3.1 Hz. The events with amplitudes approximately equal to multiples of the quantal size were, in most cells, more numerous than could be accounted for by coincidence of randomly occurring events of quantal size. 5. The results indicate that spontaneous EPSCs can reflect more than a single quantum, and suggest that quantal events may be coupled due to action potential‐independent near‐synchronous multiquantal release of transmitter.

[1]  B. Sakmann,et al.  Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. , 1992, The Journal of physiology.

[2]  J. Bornstein Spontaneous multiquantal release at synapses in guinea‐pig hypogastric ganglia: evidence that release can occur in bursts. , 1978, The Journal of physiology.

[3]  S. Sherman,et al.  Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[4]  D. Daley,et al.  Statistical analysis of synaptic transmission: model discrimination and confidence limits. , 1994, Biophysical journal.

[5]  S. Sherman,et al.  Synaptic circuits involving an individual retinogeniculate axon in the cat , 1987, The Journal of comparative neurology.

[6]  A. W. Liley Spontaneous release of transmitter substance in multiquantal units , 1957, The Journal of physiology.

[7]  D Ulrich,et al.  Miniature excitatory synaptic currents corrected for dendritic cable properties reveal quantal size and variance. , 1993, Journal of neurophysiology.

[8]  N. Spruston,et al.  Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. , 1993, Journal of neurophysiology.

[9]  P Heggelund,et al.  The quantal size at retinogeniculate synapses determined from spontaneous and evoked EPSCs in guinea‐pig thalamic slices. , 1994, The Journal of physiology.

[10]  R. Malinow,et al.  Direct measurement of quantal changes underlying long-term potentiation in CA1 hippocampus , 1992, Neuron.

[11]  A. R. Martin,et al.  The end‐plate potential in mammalian muscle , 1956, The Journal of physiology.

[12]  Calvin L. Williams,et al.  Modern Applied Statistics with S-Plus , 1997 .

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

[14]  D. Kullmann,et al.  Applications of the expectation-maximization algorithm to quantal analysis of postsynaptic potentials , 1989, Journal of Neuroscience Methods.

[15]  E. McLachlan The statistics of transmitter release at chemical synapses. , 1978, International review of physiology.

[16]  R. Silver,et al.  Rapid-time-course miniature and evoked excitatory currents at cerebellar synapses in situ , 1992, Nature.

[17]  M. C. Jones,et al.  A reliable data-based bandwidth selection method for kernel density estimation , 1991 .

[18]  N. Ropert,et al.  Characteristics of miniature inhibitory postsynaptic currents in CA1 pyramidal neurones of rat hippocampus. , 1990, The Journal of physiology.

[19]  R. Nicoll,et al.  Long-term potentiation is associated with increases in quantal content and quantal amplitude , 1992, Nature.

[20]  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.

[21]  H Korn,et al.  Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions. , 1992, Science.

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

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

[24]  S. Redman Quantal analysis of synaptic potentials in neurons of the central nervous system. , 1990, Physiological reviews.

[25]  B. Silverman,et al.  Using Kernel Density Estimates to Investigate Multimodality , 1981 .

[26]  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.

[27]  V. Crunelli,et al.  Membrane properties of morphologically identified X and Y cells in the lateral geniculate nucleus of the cat in vitro. , 1987, The Journal of physiology.

[28]  H Korn,et al.  Transmission at a central inhibitory synapse. IV. Quantal structure of synaptic noise. , 1990, Journal of neurophysiology.

[29]  J. Clements Quantal synaptic transmission? , 1991, Nature.

[30]  S. Sherman,et al.  Passive cable properties and morphological correlates of neurones in the lateral geniculate nucleus of the cat. , 1987, The Journal of physiology.

[31]  P. Andersen,et al.  Putative Single Quantum and Single Fibre Excitatory Postsynaptic Currents Show Similar Amplitude Range and Variability in Rat Hippocampal Slices , 1992, The European journal of neuroscience.

[32]  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.

[33]  D. Faber,et al.  Synaptic noise and multiquantal release at dendritic synapses. , 1993, Journal of neurophysiology.

[34]  B. Sakmann,et al.  Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. , 1993, The Journal of physiology.

[35]  S. Rapisardi,et al.  Synaptology of retinal terminals in the dorsal lateral geniculate nucleus of the cat , 1984, The Journal of comparative neurology.

[36]  H. Korn,et al.  Automatic detection of spontaneous synaptic responses in central neurons , 1994, Journal of Neuroscience Methods.

[37]  S. S. Wilks The Large-Sample Distribution of the Likelihood Ratio for Testing Composite Hypotheses , 1938 .