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The Action of Cholinergic Agonists on the Squid Stellate Ganglion Giant Synapse’

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The Action of Cholinergic Agonists on the Squid Stellate Ganglion Giant Synapse’ 0270~6474/84/0407-1904$02.00/O The Journal of Neuroscience Copyright 0 Society for Neuroscience Vol. 4, No. 7, pp. 1904-1911 Printed in U.S.A. July 1984 THE ACTION OF CHOLINERGIC AGONISTS ON THE SQUID STELLATE GANGLION GIANT SYNAPSE’ E. F. STANLEY Marine Biological Laboratory, Woods Hole, Massachusetts 02543 and Department of Neurology, Johns Hopkins School of Medicine, Baltimore, Maryland 21205 Received December 27, 1983; Revised February 28, 1984; Accepted February 28, 1984 Abstract Although the giant synapse in the squid stellate ganglion has served as a model in the understand- ing of the ionic and electrical changes that occur during the release of transmitter from nerve terminals, little is known about the pharmacology of this synapse or the identity of its neurotrans- mitter. In the present study, the suggestion that acetylcholine (ACh) is the excitatory transmitter at this synapse was tested by exploring the actions of cholinergic agents on the pre- and postsynaptic giant axons and on the excitatory postsynaptic potential (EPSP). A novel arterial perfusion technique that circumvents the diffusion barrier from the bathing medium to the synapse has been used to demonstrate a depolarizing action of ACh and its agonist carbachol on the post- but not the presynaptic axon. The cholinergic receptors are distinct from receptors activated by amino acids, such as glutamate, have a reversal potential of about -48 mV, are anion-permeable, and desensitize without blocking the EPSP. It is concluded that these receptors are involved in an inhibitory input onto the postsynaptic giant axon and, therefore, that ACh is most probably not the transmitter at the squid giant synapse. The giant synapse in the squid stellate ganglion has apse, noted by several workers (Bryant, 1958; Webb et served as a model in the study of the ionic permeability al., 1966; Kelly and Gage, 1969; Lester, 1970; Stanley changes and electrical events that are associated with and Adelman, 1982). the release of transmitter from the nerve terminal (e.g., Previous studies have proposed two substances as ex- Bullock and Hagiwara, 1957; Takeuchi and Takeuchi, citatory transmitters at this synapse: glutamate (GLU) 1962; Katz and Miledi, 1967; Kusano et al., 1967; Miledi, (Miledi, 1967) and acetylcholine (ACh) (Webb et al., 1973; Llinas and Nicholson, 1975; Llinas et al., 1981; 1966). These proposals are consistent with morphological Charlton et al., 1982). The large size of the presynaptic studies which have shown that the vesicles in the pre- axon terminal (Young, 1939), allowing direct microelec- synaptic axon terminal are large and clear (Froesch and trode recording (Bullock, 1948) and current passing, is Martin, 1972; Pumplin and Reese, 1978). The evidence the principal reason for the usefulness of this prepara- supporting GLU includes blockade (desensitization ?) of tion. In contrast, this preparation may be one of the least the excitatory postsynaptic potential (EPSP) with bath well understood preparations in terms of its pharmacol- application (Kelly and Gage, 1969) and depolarization of ogy; in particular, the transmitter active at this synapse the postsynaptic axon membrane with iontophoresis has not been identified, and little is known about the (Miledi, 1967, 1969, 1972), although the difficulty of receptors on the postsynaptic axon. The main reason the iontophoresis of agents into this preparation was noted pharmacological properties of this neurobiologically im- (see “Discussion”). However, the hypothesis that GLU portant synapse have not been explored is the substantial is the transmitter has been questioned due to the obser- diffusion barrier from the bathing medium to the syn- vation that the depolarization evoked by GLU has a different reversal poential (ER) (Miledi, 1969) from that i I am indebted to a number of individuals in the course of carrying of the EPSP (Miledi, 1969; Llinas et al., 1974). out and writing this study, including E. Aizenman and Drs. W. J. The evidence in favor of cholinergic transmission is Adelman, Jr. (National Institutes of Health Biophysics Laboratory, Marine Biological Laboratory), M. P. Charlton (University of Toronto), based on the presence of cholinesterase in the stellate S. J. Smith (Yale University), G. J. Augustine, Jr. (University of ganglion (Nachmansohn and Meyerhof, 1941; Bryant California, Los Angeles), and P. Talalay. I thank Ms. C. Barlow-Salemi and Brzin, 1966) and its localization near the giant for secretarial assistance. This work was supported by Grant R03 synapse in morphological studies (Brzin et al., 1975), and MH38359-01 from the National Institute of Mental Health. the demonstration of ACh and choline acetyltransferase 1904 The Journal of Neuroscience Action of Cholinergic Agents on the Squid Giant Synapse 1905 (CAT) in segments of the ganglion containing the giant access of microelectrodes to the pre- and postsynaptic synapse (Rosenberg et al., 1966; Webb et al., 1966). giant axons. Perfusion was achieved by forcing artificial However, cholinergic markers have also been reported in sea water (ASW, composition in millimolar concentra- non-neural cells (Heumann et al., 1981). Studies at- tion: NaCl, 423.0; KCl, 9.0; CaC12, 9.3; MgC12, 25.5; tempting to demonstrate a physiological action of ACh MgS04, 25.5; HEPES, 5.0; pH 7.2) through the ganglion at the giant synapse have resulted in, at best, inconclu- under pressure from an 02 gas tank. The preparation sive results. Application of ACh in the bathing medium was well maintained by this method; transmission con- failed to depolarize the postsynaptic axon, and synaptic tinued for several hours of study without further oxygen- transmission was blocked only after long periods of treat- ation. ment (16 to 90 min) in very high concentrations of ACh Test solutions were introduced into the ganglion by (5 x lop2 M) (Bryant, 1958; Webb et al., 1966). The manually turning the tap on a micro-stopcock (Hamil- failure of ACh to cause a physiologically detectable action ton). The test substances were housed in containers on the postsynaptic giant axon was attributed (correctly, under the same O2 pressure. With this “constant pres- see below) to the diffusion barrier (Webb et al., 1966). sure” technique, pressure changes during switching from In view of the evidence questioning GLU as the excit- one solution to another were avoided so that microelec- atory transmitter at this synapse, the present study was trode recording could be used to evaluate the effects of undertaken to re-evaluate the possible role of ACh, since the test solutions without any movement artefact. Flow all of the characteristic cholinergic markers have been rates ranged from 0.1 to 0.5 ml/min, depending in part identified in the stellate ganglion. In order to study the on leaks through small artery branches that were not action of ACh at this synapse however, it is first neces- ligatured. Experiments were carried out at room temper- sary to solve the technical problem enountered in pre- ature (22°C). vious studies, of the diffusion barrier from the bathing Stimulation and recording techniques. The prenerve medium to the giant synapse itself. We have recently was stimulated by a square wave pulse of electricity (0.1 described a novel arterial perfusion technique that cir- msec) originating from a stimulator (Grass S48) via a cumvents this barrier and allows the virtually immediate stimulus isolation unit and a pair of silver wire electrodes introduction of agents into the stellate ganglion (E. F. hooked under the nerve. Intracellular recording was car- Stanley and W. J. Adelman, Jr., 1982, and submitted for ried out by conventional microelectrode techniques. A 3 publication). The hypothesis that ACh may be the trans- M potassium chloride-filled micropipette (5 to 15 meg- mitter at this synapse was examined by testing the effect ohms) was connected by a holder and probe to a WPI of cholinergic agonists on this axon. It is shown that S7000 microelectrode amplifier. Currents were passed there are indeed cholinergic receptors on the postsyn- intracellularly by means of a second microelectrode (<lo aptic site, but that these receptors have characteristics megohms) filled with 3 M potassium acetate connected that are not consistent with ACh acting as an excitatory to a constant current output from the S7000. The ground transmitter at the squid stellate ganglion giant synapse. electrode was a heavily chlorided coil of silver wire. The output of the amplifier was displayed on a storage oscil- Materials and Methods loscope (Tektronix Dll) to record action potentials and synaptic potentials, while resting potentials were re- Experiments were carried out on small squid of mantle corded on the digital meter of the S7000. length 100 to 140 mm. The dissection, mounting, and perfusion technique have been described (E. F. Stanley and W. J. Adelman, Jr., submitted for publication) but Results are summarized below. Effect of acetylcholine and carbachol (CARB). Infusion The squid was decapitated, the mantle was cut along of ACh (1 mM) resulted in an abrupt depolarization of the ventral midline, and the internal organs, excepting the postsynaptic giant axon followed by a gradual repo- the gut, were removed. The muscle wall of the gut was larization toward the resting level (Fig. 1). Switching the cut up either side, and the gut was carefully removed, perfusion solution from ACh to CARB (1 mM) did not taking care not to damage the underlying blood vessels affect the resting membrane potential. After washout or the nerves from the cerebral ganglia. The aorta was with plain ASW, however, CARB also depolarized the cannulated caudally, close to the point where a single postsynaptic membrane. The amplitude of the depolari- branch, the common stellate artery, penetrates the gut zation was related to the concentration of CARB, and wall and bifurcates to supply the two ganglia (the right depolarizations were detected at concentrations as low and left stellate arteries). A ligature was tied on the as 0.1 mM.
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