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Junctional Transmission II. Presynaptic Mechanisms

A. R. Martin

10.1002/cphy.cp010110

Source: Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons

Originally published: 1977

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 The Quantum Hypothesis
1.1 Binomial and Poisson Statistics
1.2 Experimental Tests of Quantum Hypothesis
1.3 Measurement of Mean Quantum Content
1.4 Measurement of Release Probability and Number of Available Quanta
1.5 Experimental Values of Statistical Release Parameters at Various Junctions
2 Spontaneous Miniature Potentials
3 Synaptic Vesicles
4 Synaptic Delay
5 Depolarization and Release
6 Divalent Cations
6.1 Evoked Release
6.2 Calcium Entry
6.3 Spontaneous Release
7 Facilitation
8 Posttetanic Potentiation
9 Presynaptic Inhibition
10 Conclusion
Figure 1.

Schematic representation of basic arrangement for electrical recording from single end plates. Muscle (M) is placed in chamber and covered with appropriate saline solution. Nerve (N) placed on stimulating electrodes (S). Usually for this purpose nerve is led into oil‐filled side chamber to prevent drying (not shown). Micropipette (P) is connected to preamplifier (A), output of which is recorded on cathode‐ray oscilloscope (C). Mechanical arrangement not shown. Preparation is usually observed with a dissecting microscope and transillumination, and pipette must be carried on a suitable micromanipulator.
Figure 2.

A: spontaneous MEPP's recorded from frog muscle in normal Ringer's solution. Arrows indicate 1 mV, 20 ms. B: response recorded from end‐plate region of frog muscle to repeated nerve stimulation at arrows. Low‐Ca Ringer's solution with neostigmine bromide (1 μg/ml). Note stepwise fluctuation in EPP's on successive trials. Voltage scale, 1 mV.

From Fatt & Katz 36
Figure 3.

A: histograms of EPP and spontaneous potential amplitude distributions obtained from tenuissimus muscle of the cat. Krebs solution with 12.5 mM Mg. Peaks in EPP amplitude distribution occur at 1, 2, 3, and 4 times mean amplitude of spontaneous miniature potentials. Arrows, expected number of failures; smooth curve, expected EPP amplitude distribution. B: method of obtaining smooth curve in A. Expected single responses, double responses, and so forth calculated from Poisson equation. Expected responses are then distributed normally about mean amplitudes equal to 1, 2, … times mean amplitude of spontaneous potentials, with variances equal to same multiples of miniature potential variance.

From Boyd & Martin 14
Figure 4.

Histograms of quantum contents (x) of EJP's recorded extracellularly from crayfish neuromuscular junction. Quantum contents obtained by counting responses in records similar to those shown in Fig. 7, taken at 3°C. Black bars, experimentally observed distribution; stippled bars, expected Poisson distribution with same m; white bars, expected binomial distribution with same m and p = 0.044 (A) and 0.49 (B). m obtained by dividing total number of quanta released by number of trials, p from m, and variance of the responses (see text).

From Johnson & Wernig 50
Figure 5.

Theoretically expected decline in EPP amplitude during brief train of stimulation. Amplitude of each successive EPP vn), expressed as a fraction of initial amplitude (v1), plotted against sum of all previous amplitudes normalized in the same way. Points are successive numerical calculations assuming depletion of quantal store. A: no recovery from depletion of quanta between shocks; ○, release probability assumed constant during train; •, facilitation of release probability; Δ, depression of release probability (see text). B: same curves replotted, assuming 1% replacement of net loss of transmitter between each shock. Lines, extrapolation of linear part of curves to abscissa; intercept in such experiments is usually taken as 1/p. In all curves initial value of p is 0.2. Extrapolation approximates 1/p = 5 when p is assumed constant or facilitated but is too low if p is depressed during train

Adapted from Christensen & Martin 17
Figure 6.

A: distribution of time intervals between successive spontaneous miniature potentials in frog muscle. Observations grouped in classes of 20 ms; mean interval 221 ms. B: replot of same results, showing total number of intervals of duration less than t. Circles, observed numbers; line, expected Poisson distribution y = N(1 ‐ e−t/T), where N is total number of observations and T is mean interval.

From Fatt & Katz 36
Figure 7.

End‐plate responses (M) to nerve stimulation recorded with focal extracellular electrode. Ca‐free solution with Ca supplied locally from recording pipette. Temperature, 2.5°C. N indicates extracellular record of nerve terminal action potential. Responses consist of individual MEPP's with widely varying delay after nerve action potential. Lower record, increased Ca efflux from pipette gave rise to large end‐plate response and extracellularly recorded muscle action potential.

From Katz & Miledi 51
Figure 8.

Histograms of synaptic delays of responses such as those shown in Fig. 7, at indicated temperatures. Each experiment consisted of 250-300 observations. Minimum delay at 17.5°C approximately 0.5 ms; at 2.5°C approximately 5 ms.

From Katz & Miledi 51
Figure 9.

Excitatory postsynaptic potential (middle record) at squid giant synapse in response to depolarization of presynaptic terminal (lower record) produced by current from intracellular electrode (upper record). Recording arrangement as in Fig. 10A. Note synaptic delay between peak depolarization and EPSP. Action potentials blocked with TTX.

From Katz & Miledi 54
Figure 10.

Plot of EPSP amplitude (mV post) against presynaptic depolarization (mV pre) from experiment similar to that shown in Fig. 9. Inset A shows positions of current‐passing electrode (a), presynaptic voltage‐recording electrode (b) and postsynaptic recording electrode (c). Curve B shows relation between mV post and mV pre on linear scale; inset C shows detail of initial part of curve. Curve D is mV post plotted on a logarithmic scale against mV pre. Slope of line corresponds to a 10‐fold change on EPSP for 7.5‐mV change in presynaptic depolarization.

From Katz & Miledi 54
Figure 11.

Experiment similar to those shown in Figs. 9 and 10, but with longer duration current pulses. Action potentials blocked with TTX, and delayed rectification blocked by intracellular loading of terminal with TEA. Note that EPSP at onset of depolarization is gradually suppressed and replaced by off response at end of pulse as depolarization is increased.

From Katz & Miledi 54
Figure 12.

Relation between Ca concentration and EPP amplitude at frog neuromuscular junction at 3 different concentrations of Mg. ○, 0.5 mM Mg; +, 2 mM Mg; •, 4 mM Mg. A: linear scale. B: both coordinates logarithmic. Slope of lines on logarithmic plot is approximately 3.9.

From Dodge & Rahamimoff 27
Figure 13.

Effects of Ca and Mg on EPP's recorded intracellularly from frog muscle. Preparation bathed in Ca‐free solution with about 1 mM Mg; TTX added to block action potentials. Temperature, 5°C. Ca and Mg applied focally to the nerve terminal from a triple‐barreled pipette. A: upper record, depolarizing pulse from one barrel (P) produces small EPP; middle record, when depolarizing pulse is preceded by Ca ejected from second barrel (Ca) EPP is increased; lower record, control pulse with no Ca produces failure of response. B: sequence similar to A, but with steady leak of Ca from second barrel of pipette; Mg pulse from third barrel (Mg) before depolarization blocks EPP.

From Katz & Miledi 52
Figure 14.

Electrical response to depolarization of presynaptic terminal of squid giant synapse. Na and K currents blocked by TTX and TEA, respectively. Extracellular Ca concentration, 45 mM. A: two depolarizing current pulses (upper trace) applied to terminal. First pulse produces apparent local response which is terminated at end of pulse. Second pulse results in a regenerative response and continued depolarization after current pulse is terminated. B: similar response from another terminal on slower time base to show prolonged active depolarization of terminal (lower trace) in response to brief depolarizing pulse (upper trace). Middle trace, EPSP.

From Katz & Miledi 57
Figure 15.

A: EPP's recorded intracellularly from frog muscle during a conditioning train of 5 shocks followed by a single test shock. EPP amplitude is facilitated during train and in subsequent test period. Stimulus interval in train, 20 ms. B: averaged responses from another end plate; 8 superimposed plots, each with different test interval and each representing average of 50 responses similar to that shown in A. Facilitation is maximum after train and decays as test interval is lengthened.

From Mallart & Martin 71
Figure 16.

Intracellular records from crayfish neuromuscular junction. A: EJP produced by stimulation of excitatory nerve. C: IJP produced by inhibitory nerve stimulation. Reversal potential for IJP is indicated by Rev. pot. B: combined stimulation, so that EJP and IJP are superimposed, produces little change in EJP amplitude. D: EJP is markedly suppressed when inhibitory stimulation precedes excitatory stimulation by about 3 ms. Note that IJP is almost terminated before beginning of EJP.

From Dudel & Kuffler 32


Figure 1.

Schematic representation of basic arrangement for electrical recording from single end plates. Muscle (M) is placed in chamber and covered with appropriate saline solution. Nerve (N) placed on stimulating electrodes (S). Usually for this purpose nerve is led into oil‐filled side chamber to prevent drying (not shown). Micropipette (P) is connected to preamplifier (A), output of which is recorded on cathode‐ray oscilloscope (C). Mechanical arrangement not shown. Preparation is usually observed with a dissecting microscope and transillumination, and pipette must be carried on a suitable micromanipulator.



Figure 2.

A: spontaneous MEPP's recorded from frog muscle in normal Ringer's solution. Arrows indicate 1 mV, 20 ms. B: response recorded from end‐plate region of frog muscle to repeated nerve stimulation at arrows. Low‐Ca Ringer's solution with neostigmine bromide (1 μg/ml). Note stepwise fluctuation in EPP's on successive trials. Voltage scale, 1 mV.

From Fatt & Katz 36


Figure 3.

A: histograms of EPP and spontaneous potential amplitude distributions obtained from tenuissimus muscle of the cat. Krebs solution with 12.5 mM Mg. Peaks in EPP amplitude distribution occur at 1, 2, 3, and 4 times mean amplitude of spontaneous miniature potentials. Arrows, expected number of failures; smooth curve, expected EPP amplitude distribution. B: method of obtaining smooth curve in A. Expected single responses, double responses, and so forth calculated from Poisson equation. Expected responses are then distributed normally about mean amplitudes equal to 1, 2, … times mean amplitude of spontaneous potentials, with variances equal to same multiples of miniature potential variance.

From Boyd & Martin 14


Figure 4.

Histograms of quantum contents (x) of EJP's recorded extracellularly from crayfish neuromuscular junction. Quantum contents obtained by counting responses in records similar to those shown in Fig. 7, taken at 3°C. Black bars, experimentally observed distribution; stippled bars, expected Poisson distribution with same m; white bars, expected binomial distribution with same m and p = 0.044 (A) and 0.49 (B). m obtained by dividing total number of quanta released by number of trials, p from m, and variance of the responses (see text).

From Johnson & Wernig 50


Figure 5.

Theoretically expected decline in EPP amplitude during brief train of stimulation. Amplitude of each successive EPP vn), expressed as a fraction of initial amplitude (v1), plotted against sum of all previous amplitudes normalized in the same way. Points are successive numerical calculations assuming depletion of quantal store. A: no recovery from depletion of quanta between shocks; ○, release probability assumed constant during train; •, facilitation of release probability; Δ, depression of release probability (see text). B: same curves replotted, assuming 1% replacement of net loss of transmitter between each shock. Lines, extrapolation of linear part of curves to abscissa; intercept in such experiments is usually taken as 1/p. In all curves initial value of p is 0.2. Extrapolation approximates 1/p = 5 when p is assumed constant or facilitated but is too low if p is depressed during train

Adapted from Christensen & Martin 17


Figure 6.

A: distribution of time intervals between successive spontaneous miniature potentials in frog muscle. Observations grouped in classes of 20 ms; mean interval 221 ms. B: replot of same results, showing total number of intervals of duration less than t. Circles, observed numbers; line, expected Poisson distribution y = N(1 ‐ e−t/T), where N is total number of observations and T is mean interval.

From Fatt & Katz 36


Figure 7.

End‐plate responses (M) to nerve stimulation recorded with focal extracellular electrode. Ca‐free solution with Ca supplied locally from recording pipette. Temperature, 2.5°C. N indicates extracellular record of nerve terminal action potential. Responses consist of individual MEPP's with widely varying delay after nerve action potential. Lower record, increased Ca efflux from pipette gave rise to large end‐plate response and extracellularly recorded muscle action potential.

From Katz & Miledi 51


Figure 8.

Histograms of synaptic delays of responses such as those shown in Fig. 7, at indicated temperatures. Each experiment consisted of 250-300 observations. Minimum delay at 17.5°C approximately 0.5 ms; at 2.5°C approximately 5 ms.

From Katz & Miledi 51


Figure 9.

Excitatory postsynaptic potential (middle record) at squid giant synapse in response to depolarization of presynaptic terminal (lower record) produced by current from intracellular electrode (upper record). Recording arrangement as in Fig. 10A. Note synaptic delay between peak depolarization and EPSP. Action potentials blocked with TTX.

From Katz & Miledi 54


Figure 10.

Plot of EPSP amplitude (mV post) against presynaptic depolarization (mV pre) from experiment similar to that shown in Fig. 9. Inset A shows positions of current‐passing electrode (a), presynaptic voltage‐recording electrode (b) and postsynaptic recording electrode (c). Curve B shows relation between mV post and mV pre on linear scale; inset C shows detail of initial part of curve. Curve D is mV post plotted on a logarithmic scale against mV pre. Slope of line corresponds to a 10‐fold change on EPSP for 7.5‐mV change in presynaptic depolarization.

From Katz & Miledi 54


Figure 11.

Experiment similar to those shown in Figs. 9 and 10, but with longer duration current pulses. Action potentials blocked with TTX, and delayed rectification blocked by intracellular loading of terminal with TEA. Note that EPSP at onset of depolarization is gradually suppressed and replaced by off response at end of pulse as depolarization is increased.

From Katz & Miledi 54


Figure 12.

Relation between Ca concentration and EPP amplitude at frog neuromuscular junction at 3 different concentrations of Mg. ○, 0.5 mM Mg; +, 2 mM Mg; •, 4 mM Mg. A: linear scale. B: both coordinates logarithmic. Slope of lines on logarithmic plot is approximately 3.9.

From Dodge & Rahamimoff 27


Figure 13.

Effects of Ca and Mg on EPP's recorded intracellularly from frog muscle. Preparation bathed in Ca‐free solution with about 1 mM Mg; TTX added to block action potentials. Temperature, 5°C. Ca and Mg applied focally to the nerve terminal from a triple‐barreled pipette. A: upper record, depolarizing pulse from one barrel (P) produces small EPP; middle record, when depolarizing pulse is preceded by Ca ejected from second barrel (Ca) EPP is increased; lower record, control pulse with no Ca produces failure of response. B: sequence similar to A, but with steady leak of Ca from second barrel of pipette; Mg pulse from third barrel (Mg) before depolarization blocks EPP.

From Katz & Miledi 52


Figure 14.

Electrical response to depolarization of presynaptic terminal of squid giant synapse. Na and K currents blocked by TTX and TEA, respectively. Extracellular Ca concentration, 45 mM. A: two depolarizing current pulses (upper trace) applied to terminal. First pulse produces apparent local response which is terminated at end of pulse. Second pulse results in a regenerative response and continued depolarization after current pulse is terminated. B: similar response from another terminal on slower time base to show prolonged active depolarization of terminal (lower trace) in response to brief depolarizing pulse (upper trace). Middle trace, EPSP.

From Katz & Miledi 57


Figure 15.

A: EPP's recorded intracellularly from frog muscle during a conditioning train of 5 shocks followed by a single test shock. EPP amplitude is facilitated during train and in subsequent test period. Stimulus interval in train, 20 ms. B: averaged responses from another end plate; 8 superimposed plots, each with different test interval and each representing average of 50 responses similar to that shown in A. Facilitation is maximum after train and decays as test interval is lengthened.

From Mallart & Martin 71


Figure 16.

Intracellular records from crayfish neuromuscular junction. A: EJP produced by stimulation of excitatory nerve. C: IJP produced by inhibitory nerve stimulation. Reversal potential for IJP is indicated by Rev. pot. B: combined stimulation, so that EJP and IJP are superimposed, produces little change in EJP amplitude. D: EJP is markedly suppressed when inhibitory stimulation precedes excitatory stimulation by about 3 ms. Note that IJP is almost terminated before beginning of EJP.

From Dudel & Kuffler 32
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Article Title: Junctional Transmission II. Presynaptic Mechanisms
 

How to Cite

A. R. Martin. Junctional Transmission II. Presynaptic Mechanisms. Compr Physiol 2011, Supplement 1: Handbook of Physiology, The Nervous System, Cellular Biology of Neurons: 329-355. First published in print 1977. doi: 10.1002/cphy.cp010110