THE ACTION OF DRUGS, ESPECIALLY ACETYL- CHOLINE, ON THE ANNELID BODY WALL {LUMBRICUS, ARENICOLA)
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1 VOL. XVI, No. 3 JULY, 1939 THE ACTION OF DRUGS, ESPECIALLY ACETYL- CHOLINE, ON THE ANNELID BODY WALL {LUMBRICUS, ARENICOLA) BY K. S. WU From the Department of Zoology, University College, London [Received n October 1938) (With Three Text-figures) IN the course of a recently published investigation (Wu, 1939) it was found that the gut of the earthworm differed from the well-known preparation of the dorsal musculature of the leech (Fiihner, 1918; Minz, 1932), as regards its reactions to acetylcholine, in the following respects: (1) in the absence of eserine the body wall of the leech is very much less sensitive to acetylcholine than is the gut (crop and gizzard) of the earthworm, the lowest effective concentration of the drug being io" 4 to io" 5 for the former and io~ B to io- 10 for the latter; (2) treatment with eserine increases the sensitivity to acetylcholine of the leech dorsum enormously and that of the earthworm gut only slightly, so that the former (lowest effective concentration io~ 8 to io" 10 ) is now nearly as sensitive as the latter (io~ 10 to io~ u ); (3) adopting the classification of Dale (1914), the action of acetylcholine on the leech is a "nicotine-action" (abolished by large doses of nicotine) while that on the earthworm gut is a " muscarine-action " (abolished by small doses of atropine). The question therefore arises, are these differences due to the fact that we are dealing with two species, earthworm and leech, or with two organs, body wall and gut? To answer this question, the writer has studied the action of acetylcholine and certain other relevant drugs on the body wall of the earthworm (Lumbricus terrestris) and of the lugworm (Aremcola marina). By putting these results beside those already established for the leech, a comparison can be drawn between the reactions of the body wall in representatives of all of the three great divisions of the annelid phylum. As regards the gut, the data of Wu (1939) on the earthworm and of Wells (1937) on the lugworm are also available for comparison. MATERIAL Most of the experiments were done on longitudinal strips including tissue from several segments of the worm. In Lumbricus, either dorsal, ventral or lateral strips were used. All of these strips showed spontaneous rhythmic activity, whether they contained the ventral nerve cord or not. In Arenicola, the strips were ventral, dorsal or ventro-lateral; in the latter case the ventral nerve cord was present in some jeb-xviiii 17
2 252 K. S. Wu experiments and absent in others. In contrast to the earthworm strips, those of Arenicola only showed spontaneous activity if the ventral nerve cord was present. The ventral strips were very active and often showed outbursts of rhythmic activity alternating with more quiet periods, rather like the behaviour pattern of the isolated oesophagus and extrovert preparations of Wells (1937) but not so regular. In addition to the longitudinal strips, experiments were also made on circular strips of Arenicola body wall. Rings were cut including two or three segments and converted into strips by dividing them in the mid-dorsal line. The oblique muscles were also cut through. These strips showed a very regular continuous rhythm. ESERINE It was found that eserine alone exerted a striking exciting action on the earthworm body wall (Fig. 1). The effect is shown by dorsal, ventral and lateral strips, Fig. 1. Lateral strip of the earthworm (Lumbricus terrestris). The record begins in Ringer, at signal eserine io~* is added. In all records: read from left to right; upstroke of lever means shortening of preparation; time signal marks once a minute. and can be detected even with concentrations of eserine down to io~ 7. In the case of Arenicola, the effect is seen only in the case of longitudinal strips containing the nerve cord. The dorsal and lateral strips, which showed no spontaneous rhythm, were not excited by eserine; neither were the circular strips, although they contained nerve cord and were spontaneously rhythmic.
3 Action of Drugs on the Annelid Body Wall 253 ACETYLCHOLINE The characteristic effect of acetylcholine on all the annelid muscles under consideration (body wall or gut) is the evocation of a swift tonic contraction. In all the earthworm and lugworm strips, the concentration of acetylcholine required to produce a contraction in the absence of eserine is from 10-4 to io" 5 ; they therefore quantitatively resemble the leech body wall in this respect. Moreover, eserine greatly sensitizes the earthworm and lugworm body wall to acetylcholine, the effect being nearly, but not quite, as great as in the leech. Eserine was applied in the following concentrations: io~ 6 or io~ 7 for the earthworm and io~ B or 1/5 x io~* for Arenicola. After eserine, the lowest effective concentrations of acetylcholine were found to be io~ 6 to io~ 8 for Lumbricus, io~ 9 for Arenicola when the strips were longitudinally ventral and io~ 7 to io~* for Arenicola for longitudinally dorsal and circular strips, a8 compared with io" 8 to io~ 10 for the leech. ATROPINE It was shown previously (Wu, 1939) that atropine from 1 : 5000 to io~ B has a slight exciting action, and can abolish the action of acetylcholine, on the earthworm gut. On the earthworm body wall, atropine io~ B has a slight excitatory action and reduces the response to acetylcholine, but does not completely abolish it. Similarly the sensitivity to acetylcholine of the longitudinal and circular strips of Arenicola body wall is reduced by previous application of atropine io~ s but the response is not abolished altogether by atropine either in this concentration or 1/5 x io" 4. The annelid body wall seems to resemble the rectus abdominis of the frog, in which the response to acetylcholine is diminished but not abolished by atropine (Riesser & Neuschloss, 1921; Bfown, 1937). NICOTINE Both in the earthworm and in the lugworm, nicotine by itself causes contraction of the body wall. In Lumbricus, nicotine io~ B causes a single, quick twitch-like contraction followed by slow relaxation. In Arenicola, with high concentrations (io~ 3 to 10-4 ) there are two contractions first a quick rise and fall, and then a slow contraction and relaxation (Fig. 2). The first, quick, contraction seems to be due to an action of the drug on the nerves. It is much more powerful in strips which contain the nerve cord than in those which do not. With lower nicotine concentrations only the slow phase is seen. Both in Lumbricus and in Arenicola, the action of acetylcholine can be abolished by high nicotine concentrations. In Lumbricus, nicotine io~* was found to abolish the action of acetylcholine (io~ 3 without eserine). In Arenicola, nicotine 10-4 or io~ 3 completely antagonizes low concentrations of acetylcholine (io~ 6 with eserine). 17-3
4 254 K. S. Wu Higher acetylcholine concentrations now evoke a slow tone rise, quite unlike the swift normal response to the drug (Fig. 2), Fig. 2. Strips of the lugworm (Aremcola marina). A, ventro-lateral atrip, without nerve cord, 7-11 segments. The record begins in sea water, at signal nicotine io" 4 is added. B, dorsal strip, posterior third. The record begins in eserine io~* in sea water, at signal the game and acetylcholine 10"' is added. C, continuation of B. The record is taken after the preparation has been paralysed by nicotine io~*. Beginning is in nicotine io"' and eserine io~', at first signal Ach io~* + nicotine 10"' +eserine io~* and at second signal Ach io~* + nicotine io~* + e»erine io~* are applied, at third signal sea water. ADRENALINE Although the main object of these experiments was to elucidate the action of acetylcholine, experiments were also made on the action of adrenaline on the Arenicola body wall. It was shown by Wells (1937) that adrenaline inhibits the rhythm of a circular muscle strip. This result was confirmed. The inhibition is very clear and constant. It is diminished, but not abolished, by ergotoxine 1/5 x io~*. The action of adrenaline on the longitudinal strips was not so clear. The dorsal strips, which show no spontaneous rhythm, responded by loss of tone to adrenaline application in some experiments; in others, there was no definite effect. The spontaneously active ventral strip was inhibited by adrenaline in some experiments, but clearly excited in others (Fig. 3). This variability of behaviour can be attributed to the complexity of the preparation and the number of points at which the drug could act.
5 Action of Drugs on the Annelid Body Wall 255 Fig. 3. Ventral strip of the lugworrri, segments. The record (above) begins in sea water, at signal adrenaline io~ 5 is applied. The lower continues in adrenaline io~', at first signal adrenaline 1 : 80,000 is added, at second signal return to sea water. DISCUSSION Two questions may be discussed: (1) the contrast between gut and body wall, and (i) differences between the three species of worms. (1) It is clear that the three body walls (Hirudo, Lumbricus, Arenicold) differ from the earthworm gut in two respects. First, in the body wall there is a factor probably a high concentration of choline esterase which blocks the action of acetylcholine and is antagonized by eserine. All three are relatively insensitive to acetylcholine alone, and greatly sensitized by eserine. The earthworm gut, on the other hand, is very sensitive to acetylcholine alone and eserine only causes a slight increase in sensitivity. The Aremcola gut seems to resemble that of Lumbricus in this regard. Working with the front part of the lugworm gut ("isolated extrovert"), Wells (1937, and private communication) found that acetylcholine alone was effective down to about io~ 8 and that eserine only lowered the threshold to about io~ 7. Second, the action of acetylcholine on the body wall is a
6 256 K. S. Wu "nicotine action", while that on the gut, of the earthworm at least, is a '' muscarine-action''. In both points, the annelid body wall resembles vertebrate skeletal muscle while the annelid gut resembles the mammalian intestine. According to Dale & Gasser (1926), Matthes (1930), Euler & Gaddum (1931), Chang & Gaddum (1933), Gaddum (1935) and Brown (1937), the action of acetylcholine on the cat's gastrocnemius and the frog's rectus abdominis is a "nicotine action", while that on the rabbit's intestine is a "muscarine action". Moreover, the lowest effective concentration of acetylcholine without eserine is much higher in skeletal muscle (frog's rectus abdominis) than in the intestine, and the potentiating action of eserine is much greater in the former than in the latter. It is interesting that the pharmacological contrast between somatic and visceral muscle apparently applies to animals of both phyla. In this connexion, the conclusion of Riesser (1933), that the reactions to drugs of the somatic muscles of a number of invertebrates bear a general resemblance to those of vertebrate skeletal muscle, is worth pointing out. (2) On comparing the various body-wall preparations, certain points of difference appear. The most striking is the exciting effect of eserine on some of the preparations. This effect is clearly shown by the following longitudinal strips: earthworm dorsal, lateral and ventral, and Arenicola ventral. It is not shown by longitudinal dorsal strips of Arenicola or by the leech dorsum. Its incidence, as regards longitudinal strips, corresponds with the power of spontaneous rhythmic movement. However, in the Arenicola circular muscle strip, which is spontaneously rhythmic, the effect is not seen. The difference between the circular and longitudinal strips in Arenicola is also brought out by the experiments with adrenaline, which invariably depresses the circular strip but may excite the longitudinal ventral. SUMMARY 1. The actions of certain drugs (acetylcholine, eserine, atropine, nicotine, adrenaline) on strips of the body wall of the earthworm (Lumbricus terrestris) and lugworm (Arenicola marina) are described. 2. The body wall of the earthworm and lugworm resembles the dorsum of the leech, and also vertebrate skeletal muscle, in the following points: relatively insensitive to acetylcholine alone, sensitivity to acetylcholine greatly increased by eserine, response to acetylcholine abolished by nicotine. In these points, the muscles mentioned contrast with the earthworm gut and the mammalian intestine, which are: very sensitive to acetylcholine alone, sensitivity not greatly increased by eserine, response to acetylcholine abolished by atropine. 3. The various types of body wall strip differ among themselves as regards spontaneous activity, response to eserine alone, and response to adrenaline. My thanks are due to Mr G. P. Wells for his suggestion of the problem and for his continued interest throughout the investigation, and to Dr Kemp and his staff for their kindness during my visit to Plymouth, where the experiments on Arenicola were carried out.
7 Action of Drugs on the Annelid Body Wall 257 REFERENCES BROWN, G. L. (1937). J. Pkytiol. 89, 438. CHANG, H. C. & GADDUM, J. H. (1933). J. Pkytiol. 79, 255. DALB, H. H. (1914). J. Pharmacol. 6, 147. DALB, H. H. & GASSKR, H. S. (1926). J. Pharmacol. 29, 53. EULKR, U. S. & GADDUM, J. H. (1931). J. Phytiol. 72, 74. FOHNKR, H. (1918). Arch. exp. Path. Pharmak. 82, 51, 81 and Biochem. Z. 92, 347. GADDUM, J. H. (1935). Aim. Rev. Bioch. 4, 311. MATTHES, K. (1930). J. Phytiol. 70, 338. MINZ, B. (193a). Arch. exp. Path. Pharmak. 168, a93. RIESSER, O. (1933). Arch. exp. Path. Pharmak. 172, 194. RIESSER, O. & NEUSCHLOSS, S. M. (1921). Arch. exp. Path. Pharmak. 91, 34a. WELLS, G. P. (1937). J. exp. Biol. 14, 117. Wu, K. S. (1939). J. exp. Biol. 16, 2.
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