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Review a Short History of Synapses and Agonist-Activated Ion Channels View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Neuron, Vol. 20, 381±387, March, 1998, Copyright 1998 by Cell Press From Muscle Endplate to Brain Synapses: Review A Short History of Synapses and Agonist-Activated Ion Channels David Colquhoun* and Bert Sakmann² A. V. Hill was, at the time, an undergraduate of Trinity *Department of Pharmacology College Cambridge, though he later held the Chair of University College London Biophysics at University College London, in which job Gower Street he was succeeded by Bernard Katz. Hill's ideas were London WC1E 6BT developed over the next 30 years by A. J. Clark (e.g., United Kingdom Clark, 1933) and were extended to competitive antago- ² Max Planck Institut fuÈ r Medizinische Forschung nists at equilibrium by John Gaddum (e.g., Gaddum, Jahn-Strasse 29 1937) and Heinz Schild (all three of whom held the Chair 69120 Heidelberg of Pharmacology at University College London). Federal Republic of Germany There was, of course, no hint in 1878 that these obser- vations had anything to do with synaptic transmission. That idea was developed by Henry Dale and his col- Introduction leagues and was well established by the 1930s, through This review gives a very personal view of some of the classical papers such as Dale, Feldberg, and Vogt work that has led up to the present state of knowledge (1936). This done, the way was paved for the study of about synapses and ion channels. It would take a whole agonist-activated ion channels, which had its roots in book to do justice to this topic, and we can only apolo- the 1940s and 1950s, although they were not called ion gise in advance for failing to mention by name most of channels until later. Since then, we have learned how the people who have played an important part. Many of to measure the current flow through channels, we have the ªnewº ideas that are proclaimed daily are actually learned much about the rates at which agonists bind quite old, and it is perhaps appropriate to remind the and channels open and shut, and we know the primary present generation of neuroscientists of how current structure of many channels and the shape of one of views have evolved. A surprising number of them can them (Unwin, 1995). But we still do not know in any detail be found in the prescient work of Bernard Katz and his how the function of a receptor relates to its structure,nor colleagues at University College London, to whom this how exactly the agonist causes the structural re- article is a tribute. Katz made fundamental contributions arrangement that is involved in opening and shutting. to both presynaptic (transmitter release) and postsynap- Work on synaptic transmission in the brain, which had tic (ion channel) aspects of synaptic transmission. We been pioneered by Eccles and others (see Eccles, 1964), shall concentrate on the latter, and Erwin Neher will underwent an enormous explosion after the introduction discuss presynaptic events in the next review. of brain slices and the patch clamp. We are now ap- The idea of a receptor originated in the nineteenth proaching the end of the ªdecade of the brain,º and century, from the work of Paul Ehrlich and J. N. Langley. despite a great deal of interesting work and a lot of talk, Langley studied the actions of atropine and pilocarpine, it cannot honestly be said that there has been any great and in 1878 he noted (in the first volume of the Journal conceptual advance on the major issues; at the end of of Physiology, which he founded) that the inhibitory ac- the decade, we not only still do not understand memory, tion of atropine could be overcome by increasing the but we still do not understand even long term potentia- dose of pilocarpine. Moreover, the restored response tion. Perhaps it should have been a ªcentury of the to pilocarpine could in turn be abolished by further atro- brain.º What has been achieved is a considerable in- pine. Commenting on these results, Langley wrote: crease in the understanding of individual synapses in the brain. In some ways, they have turned out to be ªWe may, I think, without too much rashness, assume quite similar to the neuromuscular junctionÐvery brief that there is some substance or substances in the pulses of transmitter open postsynaptic ion channels, nerve endings or [salivary] gland cells with which both which depolarise or hyperpolarise the postsynaptic cell, atropine and pilocarpine are capable of forming com- and the time course of events is controlled largely by pounds. On this assumption, then, the atropine or the rates of binding and opening of the receptor channel pilocarpine compounds are formed according to molecule itself. In other ways, though, central synapses some law of which their relative mass and chemical are vastly more complicated. affinity for the substance are factors.º If we replace mass by concentration, the second sen- Early Work on Synaptic Transmission in Muscle tence can serve as well today as when it was written. The first estimate of the time course of transmitter action Later, Langley (1905) coined the term ªreceptive sub- was derived from measurements of the rise and decay stanceº for what we would now call a nicotinic acetyl- time course of the extracellularly recorded endplate po- choline receptor. The first quantitative treatment of this tential and from double pulse experiments (Eccles et problem was by A. V. Hill who, in 1909, gave the first al., 1941). It was correctly inferred that the permeability derivation of the Langmuir equation (10 years before change following a nerve impulse lasted only a few milli- Langmuir). He derived the result in order to try to make seconds. sense of his results on the rate of action of nicotine The 1950s saw a rapid development in the under- and curari (sic) on nicotinic acetylcholine receptors (a standing of the electrical events at synapses, in the wake problem, incidentally, that is still not entirely solved). of the elucidation of the action potential mechanism by Neuron 382 Hodgkin and Huxley in 1952. The discovery of the ideas of del Castillo and Katz (1957) gave a more con- quantal release of acetylcholine from motor nerves by crete interpretation of how an agonist could open a Paul Fatt and Bernard Katz (1950, 1951, 1952) quickly channel. led to a better understanding of transmitter release. The nature of the change in permeability to ions that was caused by acetylcholine also gave rise to much discus- The First Approach to Single Channels: sion. Fatt and Katz (1951) had suggested that acetylcho- Noise Analysis line may ªshort-circuitº the membrane, ªi.e. create aque- In the early 1970s, the advent of noise analysis (Katz ous channels through which small ions can pass without and Miledi, 1970, 1971, 1972) allowed the first (indirect) distinction,º and ª[i]t appears from these experiments inferences about the properties of single ion channels. that ACh raises both the Na and K conductance of the In the 1970 paper, Katz and Miledi showed fluctuations endplate and possibly also allows its permeability to of the response to acetylcholine that were so obvious other free ionsº (quoted from del Castillo and Katz, that one wondered why nobody had noticed them be- 1956). The definitive demonstration of the nicotinic re- fore. Katz and Miledi suggested, correctly, that the fluc- ceptor as a nonselective cation channel was achieved tuations were caused by the random opening and shut- by Takeuchi and Takeuchi (1960), in one of the first ting of individual ion channels, and used the amplitude applications of the voltage-clamp method to the end- of the fluctuations to estimate that the elementary depo- plate. larisation elicited by ACh was about 0.3 mV in amplitude. The interpretation of ion channel behaviour entered a For the first time, there was a firm estimate of the number new era when del Castillo and Katz (1957) postulated of channels opened by a single quantum of ACh. Katz the first realistic kinetic mechanism for agonist action and Miledi (1971, 1972) went on to exploit the temporal (discussed in more detail below). In the same year, Katz characteristics of the noise to estimate the duration of and Thesleff (1957) used brief iontophoretic pulses of elementary events, as well as their amplitude. By plotting acetylcholine to the endplate for the first quantitative the distribution of frequencies in the fluctuations as a investigation of nicotinic receptor desensitisation. They power spectrum, they were able to conclude, for exam- concluded that a cyclic mechanism was needed to ex- ple, that the channel that appeared after denervation plain their observations, and almost every investigation had a longer mean open time than the adult channel, of desensitisation since then has used some variant of and that carbachol produced briefer openings than ACh. their scheme. They were also able to estimate the single channel con- ductance as being of the order of 100 pS, within a factor of 3 of the value subsequently found by single channel Developments in Ideas about Receptors channel measurements. This was far bigger than some Almost half a century passed after Hill's astonishing previous biochemical estimates had suggested, and it paper was published before the next critical develop- finally settled the long-running discussion about whether ment took place. This development was the recognition the receptor was a pore or a carrier. that the binding of an agonist to a receptor, and the Soon afterwards, it was shown that inhibition of ace- subsequent activation of the receptor, had to be treated tylcholinesterase did not change the elementary event as two separate steps if any sense were to be made of but that the duration of miniature synaptic currents was the experimental results (Stephenson, 1956; del Castillo greatly increased (Katz and Miledi, 1973).
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