1. In response to stimuli at the head, a peristaltic wave travelling in any part of the earthworm’s body may be arrested. This occurs after an interval of about 0-5 sec., if the nearest part of the wave is 5 cm. from the point of stimulus. This response is of regular occurrence, and it depends on the continuity of the nerve cord between the point of stimulus and the region of the wave. It is therefore named the reflex arrest of peristalsis.

  2. The arrest of peristalsis is brought about by the complete cessation of movement of both the elongation phase and the shortening phase of the wave. The shape of the wave is not lost; though it appears that there may be some relaxation of the circular muscles in the region of elongation.

  3. The receptors of the reflex lie on the cephalic half of the body. Stimuli applied on the most cephalic one-third of the body may arrest a peristaltic wave cephalic to their point of application.

  4. The response may appear in answer to mechanical or to chemical stimuli. It may also appear in response to the absence of contact with the substratum in the head region. In this last case the reflex depends upon the presence of the supra-oesophageal ganglion. The response to mechanical stimuli, however, depends neither on the presence of the cephalic one-third of the body, nor on the presence of the tail segments.

  5. A similar reflex arrest of anti-peristalsis occurs in response to mechanical or chemical stimuli on the caudal half of the body. The time interval between stimulus and response at 5 cm. from the point of stimulus is about 0·4 sec. The anti-peristaltic wave was not observed to be arrested while travelling in the most cephalic one-third of the body.

  6. The arrest of the anti-peristaltic wave is due, too, to a cessation of movement of both phases of the wave, without a loss of its general shape.

  7. The receptors for the reflex lie in the caudal half of the body, and the nerve paths from them run in both directions. The reflex does not depend on the presence of either the head or the tail segments. It can be obtained in a worm with the most caudal one-third of the body removed, or in a worm with the most cephalic one-third cut off.

  8. The arrest of an anti-peristaltic wave by the development of a peristaltic wave can be observed in the spontaneous reversal of the direction of crawling. This act of behaviour, which is named the spontaneous immobilisation of anti-peristalsis, does not depend on the presence of either the most cephalic one-third or the most caudal one-third of the body. Though this act of. behaviour need not be considered as a reflex, its performance depends on the continuity of the nerve cord between the new peristaltic wave and the anti-peristaltic wave that is immobilized.

  9. The above three acts of behaviour are distinct from each other in their paths in the cord, and the two reflexes are distinct in their receptors. All three play an important part in one or more larger patterns of behaviour. All are conducted in paths separate from those conducting the rapid shortening reflexes.

  10. There is little evidence to throw light on the mode of action of these three immobilizations. They may be compared to the “freezing” of movement into posture found in insects and vertebrates. It is to be expected that their mechanism will prove to lie within thé central nervous system.

In the earthworm, locomotion is effected by a slowly travelling wave of thinning and elongation, followed by a wave of thickening of the body. This is generally described as a peristaltic wave. At any one moment, a whole peristaltic wave does not involve more than a part of the body of the worm. The thinning phase of the wave is produced by a local contraction of the circular musculature of the body wall; a contraction which travels along the body from head to tail at a rate of between 3 and 10 cm. per sec. (Bovard, 1918). The thickening phase of the wave, which follows the thinning, consists of a contraction of the longitudinal musculature of the body wall, travelling at about the same rate. The whole movement has recently been analysed by Gray and Lissmann (1938). The worm is capable of crawling backwards by means of a movement of the same type, the wave travelling in the reverse direction, and usually described as anti-peristalsis.

The time taken for a peristaltic wave to pass along the whole body is from about 3 to 7 sec. A worm presented with a noxious stimulus at the head, soon after a peristaltic wave has begun, would continue to crawl for some seconds subsequently towards the point of danger, were it not provided with a nervous mechanism arresting the movement of the peristaltic wave, and with mechanisms effecting its escape. Three types of immobilization of the locomotory movements (two of which for reasons given later have been called reflexes), occur as part of the natural behaviour of the worm. In the following description of them and in subsequent sections of this paper, the terms “cephalic” and “head” are used rather than “anterior”, and the terms “caudal” and “tail” are used rather than “posterior”. Thus, instead of speaking of the “anterior one-third” of the body, the segments running from the prostomium to the last segment of the clitellum are referred to as the “cephalic one-third” of the body, and so on.

(1) The reflex arrest of a peristaltic wave

When a worm is crawling head first, the application of mechanical or chemical stimuli to the cephalic one-third of the body may result in an immobilization of the peristaltic wave, which is travelling tailwards. This immobilization, occurring about 0’5 sec. after application of the stimulus, results from a halting of the thinning and thickening phases of the wave, wherever they are travelling in the body, without the characteristic shape of the peristaltic wave disappearing. There are four possible futures for the halted peristaltic wave: (i) In certain circumstances it may, after an indefinite period, travel on again towards the tail; (ii) It may remain halted until engulfed in a new peristaltic wave travelling down from the head ; (iii) It may be obliterated by the progression tailwards of the thickening phase of the wave alone; (iv) A thickening wave may appear at the caudal end of the thinning phase of the halted wave, this new wave of contraction travelling along the body towards the head.

(2) The reflex arrest of an anti-peristaltic wave

While a worm is crawling tail first, stimuli applied to the caudal half of the body may bring the anti-peristaltic wave to a halt, after an interval of about 0-4 sec., in a way similar to that described above. This arrest can take place at a considerable distance from the point of stimulation, but it has not been observed to take effect on the anti-peristaltic wave while the latter is travelling in the extreme cephalic region of the body. This response is normally accompanied by the appearance of a peristaltic wave at the head, which engulfs, on its course to the tail, the immobilized antiperistaltic wave. On other occasions a wave of longitudinal muscular contraction, running towards the head, appears and obliterates the arrested anti-peristaltic wave.

(3) The spontaneous immobilization of the anti-peristaltic wave

During its course, an anti-peristaltic wave can sometimes be observed to halt spontaneously. This halt is associated nearly always with the synchronous development of a peristaltic wave at the head. The immobilized wave is subsequently engulfed by the new peristaltic wave as it travels tailwards.

Although the mechanism of these arrests is not known to depend on nervous inhibition, it will be of some value to summarize those observations on inhibition, or supposed inhibition, that have previously been made in Lumbricus. Before the publication of a paper by Garrey & Moore in 1915, no detailed reference to the role of inhibition in the “nervous economy” of the earthworm can be traced. Garrey & Moore (1915) described a relaxation of each muscle set—the longitudinal and the circular—during the contraction of the antagonist. It was reported by Knowlton & Moore (1917) that this reciprocal relaxation was abolished by the action of strychnine, and they compared it to the reciprocal inhibition of the antagonistic muscle found in the Vertebrates.

Von Holst (1932) recently published a paper in which he claimed that an inhibitory mechanism played a very important role in the nervous economy of the earthworm. He put forward the hypothesis that, in each segmental ganglion of the nervous system there exists an inhibitory centre, whose activity prevents the spontaneous contraction of the muscles in that segment.

“The hypothesis is made, that in each ganglion there is an ‘inhibitory centre’….This ‘inhibitory centre’ is excited through the sensory endings of the skin (and often also of the musculature). If a segment is actively or passively made thinner, there occurs a specific reflex, evoked by the stimulus of thinning, in which the excitation caused by the stimulus flows into the next ganglion behind, and there opposes the effect of the inhibitory stimuli. The action of the ‘inhibitory centre’ is stopped, and the inhibition is extinguished : in short, the inhibition is inhibited…. In each ganglion there occurs, after the extinction of the inhibition, the same rhythmical event—first the contraction of the circular musculature, then the contraction of the longitudinal musculature.”

The above is a free translation of the passage (pp. 572–3) in which von Holst advances his hypothesis. He bases his assumption on a number of experiments. He found that the rate at which excitation of a peristaltic movement was conducted along the nerve cord was considerably greater than normal in a length of cord which had been separated from the body wall by cutting the lateral nerves. He reports that, if a part of the body is stretched artificially, the peristaltic wave traverses that area more rapidly than is normal. If, on the other hand, a length of the body is prevented as nearly as possible from moving; the peristaltic wave is not conducted past it. Von Holst also reports that the waves of thinning and thickening travel extremely fast over the body of a worm in a certain stage of ether anaesthesia. This he attributes to the more rapid action of ether on the “inhibitory centre” than on any other part of the ganglion. Von Hoist’s interpretation is admittedly speculative ; the present state of our knowledge of the central nervous system of Lumbricus does not allow an exact description of behaviour in the terms of nerve physiology.

Interesting and suggestive as his views and experiments are, von Hoist’s hypothesis of “inhibitory centres” does not directly concern the present account, in which the existence of definite mechanisms that immobilize the locomotory movements is reported, without an attempt being made at present to explain them in the terms of nerve physiology.

In the above-mentioned paper the author describes two cases of the arrest of a peristaltic, wave at a point distant from a stimulus. If the cephalic region of a large piece of worm is stretched, a peristaltic wave travelling away from the stretched area may be seen to slow up momentarily. If a region in the middle of a worm is stretched, a wave of peristalsis appearing at the head may disappear. Both these are probably particular cases of the responses described in this account; but, owing to the difference in the nature of the stimuli, it is not easy to compare them to any one of the reactions here described.

The earthworm, Lumbricus terrestris, was the subject of these experiments. Where observations were made with the naked eye, the findings were confirmed upon a number of worms, kept in as nearly as possible the same external conditions. The main records were made with the cinematograph. Here I am wholly indebted to Prof. Gray, both for the method and for the, apparatus used.

The worm was placed on damp blotting paper on a porcelain plate, ruled in 2 cm. squares. Cinematograph films of the acts of behaviour were taken at a frequency of twenty exposures per sec. The speed of the camera was checked by the use of a time-marker in the picture. Stimulation was effected either by the handle or the brush of a paint-brush. The negative films were interpreted in the following manner. A series of photographs showing the required reaction was selected. Beginning at the first exposure of the series, the negative was projected on to a sheet of white paper by means of an enlarger. The fixed points on the worm’s surface, denoted by the borders of the white stripes that had been painted on it (see Pl. I, figs, 1, 2 and 3), were then marked as dots on the paper from the enlarged, projected image. The film was then moved on until the next photograph required was projected, the paper was moved slightly, and the same fixed points again recorded by dots. This process was continued for the whole length of film-selected. In some cases every picture, in others every second picture, or every third, was recorded. The resulting chart gave the position of a series of fixed points on the worm at known intervals of time. The movements were represented graphically (as in Text-figs. 3, 4, 5) by the following method.

During the course of its arrest, a peristaltic or anti-peristaltic wave would involve up to seven or eight of the fixed points along the body surface. The distances A, B, C, D, E, F, etc. between the fixed points respectively 1 and 2, 2 and 3, 3 and 4, 4 and 5, 5 and 6, 6 and 7, etc., were measured to the nearest half-millimetre, in each enlargement on the chart. A series of curves, one for each of the enlarged distances A, B, C, D, E, F, etc. was then plotted on the same time-scale, one curve above the other (see Text-figs. 3, 4, 5). In all cases the wave of movement reaches point i first and travels towards points 2–7. Thus the distance A increases as the thinning phase of peristalsis, or anti-peristalsis, approaches point 2. The distance B then begins to increase, as the thinning phase of the wave passes point 2 on its way towards point 3, and so on. The thickening phase of the wave that follows, passing point 1, causes the distance A to decrease to the resting length. Subsequently the distance B decreases likewise, and so on with C, D, etc. The curve produced for each distance consists, therefore, of a flat base-line, which ascends and falls at regular intervals as each fresh peristaltic or anti-peristaltic wave grips and passes the particular part of the worm’s body. This is seen clearly in the left-hand part of Text-fig. 5.

In plotting Text-figs. 1 and 2, the procedure was more complicated. The curve for the arrest of peristalsis was superimposed upon the curve for a normal peristaltic wave, filmed immediately before. The peristaltic immobilization, which is less sharp than the anti-peristaltic, was brought out by this means. Detailed accounts of each act of behaviour follow.

Text-fig. 1.

The immobilization of a peristaltic wave in response to a stimulus in the head region of the body. △ △ △ = normal wave. • • • = arrested wave. The black block gives the duration of the stimulus.

Text-fig. 1.

The immobilization of a peristaltic wave in response to a stimulus in the head region of the body. △ △ △ = normal wave. • • • = arrested wave. The black block gives the duration of the stimulus.

Text-fig. 2.

The brief immobilization of a peristaltic wave by a stimulus at the cephalic end of the body. Conventions as in Text-fig. 1.

Text-fig. 2.

The brief immobilization of a peristaltic wave by a stimulus at the cephalic end of the body. Conventions as in Text-fig. 1.

(1) The typical reflex

The longitudinal and circular musculature of the body wall are mechanically antagonistic. The lengthening phase of the peristaltic wave is due to contraction of the circular musculature of the body wall; while the shortening phase is accompanied by relaxation of the circular musculature. A longitudinal slit cut in the dorsal body wall may be seen to open during the lengthening phase, in spite of the decreased diameter of the body, and to close during the shortening phase, although the body increases in diameter (Garrey & Moore, 1915). The shortening phase of the peristaltic wave is brought about by a contraction of the longitudinal musculature. A relaxation of the longitudinal musculature, unaccompanied by an appreciable change in shape of the body, follows shortly after the shortening has been effected. This can be seen by observing a transverse slit cut in the dorsal body wall : the slit may be seen to open during the elongation, and to remain open during the shortening phase of peristalsis; soon after the shortening phase is over, the transverse slit closes, while the contours of the body remain the same, thus indicating a relaxation of the longitudinal muscles without a change in shape of the shortened body.

If two marks are made on the body surface, an increase in the distance between them will indicate (where there is no passive stretch) a contraction of the circular musculature. A decrease in the distance between them will indicate a contraction of the longitudinal muscles. The passage of a series of peristaltic waves will, therefore, cause a regular increase and decrease of distance between these two points.

In Text-figs. 1 and 2 the changes in distance between two pairs of a series of fixed points are given. These figures illustrate two cases where the changes in distance between pairs of fixed points on the earthworm’s surface during a normal peristaltic wave can be compared with those occurring when the head of the worm is stroked with a paint-brush. In the latter case, the peristaltic wave is seen to be arrested during its course. The arrested wave, shown by the dots, has been super-imposed upon the normal wave occurring immediately before the application of the stimulus, and indicated in the figures by the fines of triangles. In Text-fig. 1 it will be seen that the increase in length of the region where the shortening phase is occurring (curves B and C) is abruptly stopped 0·4 sec. after the application of the brush. The elongation phase (curve E) comes to an abrupt end 0·55 sec. after application of the stimulus. The normal, full contraction is completed in neither phase of the peristaltic wave; while, in that region where the elongation is at its height (curve D), no normal shortening sets in. Curve A, however, gives the movements of a part of the body in which the wave has completed both phases in its cycle before the stimulus takes effect. In short, the result of a paint-brush stimulus at the head of the worm has been the arrest of the moving wave of peristalsis, without the disappearance of the characteristic shape which it imparts to the body. The arrest lasted in this particular case for 3·6 sec., before the application of a stimulus at the tail caused a general shortening of the body. The immobilization response, which I have called the reflex arrest of peristalsis, can be evoked regularly in normal, fresh earthworms.

Though the photographic record shows that both phases of the peristaltic wave are immobilized without the posture being lost, it is not possible to decide from such records what is the mechanism of the arrest, or the actual state of contraction of the muscles during the immobilization. The mechanism of the arrest will be discussed later. There is some, but not much, evidence to suggest that the muscles actually relax, at least partially, during the arrest, but that the posture is not lost because there are not strong enough forces tending to destroy it. A low-power microscopic examination of the films, using a ruled eyepiece, reveals that after normal reflex arrests there may be an increase in breadth of up to 10% in the region of the elongation. There is a corresponding, though smaller, decrease in length of up to 5 % in this region. A different series of observations suggests that there may be, in the immobilization, an actual relaxation of the circular musculature, without any marked change in shape of the elongated region. Dorsal longitudinal slits, about 2–3 mm. in length, were made in the body wall of ten worms. In each worm the observation of Garrey & Moore, that the slit widened during the elongation phase of peristalsis, was confirmed. In each, a peristaltic wave was then arrested, by an appropriate stimulus in the head region, while the elongation involved the area of the slit. Each time this was done, the slit could be seen to close, either wholly or partially, without the general shape of the stationary wave being lost. It was not found practicable to carry out a similar series of observations on the longitudinal musculature..

(2) Events following the reflex arrest

Several different events may follow the arrest of the peristaltic wave. Which of them actually occurs may be determined by such factors as the strength, or the type of the original stimulus, or by the state of the earthworm. In some cases the wave is only arrested momentarily. Text-fig. 2 illustrates such a case, when, after a light stimulus, the wave is arrested for a brief period and then continues its course. In other cases the wave may be arrested and remain stationary for 3 or 4 sec. before it is engulfed in a fresh wave of peristalsis travelling down from the head. Text-fig. 3 (curves B, C, D and E) illustrates this case. Alternatively, the arrested wave may be incorporated in an anti-peristaltic wave, which the stimulus had also evoked. In certain cases, while the elongation phase of the wave appears to be arrested, the longitudinal musculature continues to contract, and obliterates the peristaltic wave. Observation and the analysis of film records show that the continuing wave of longitudinal muscular contraction may run caudalwards, or it may appear at the caudal end of the elongated area and run towards the head.

Text-fig. 3.

A fresh peristaltic wave merging with a previously immobilized wave. The black block represents the duration of the inhibitory stimulus ; the vertical column represents an interval of 4 sec. without movement.

Text-fig. 3.

A fresh peristaltic wave merging with a previously immobilized wave. The black block represents the duration of the inhibitory stimulus ; the vertical column represents an interval of 4 sec. without movement.

(3) Types of stimuli effective in calling out the response

Mechanical stimuli, such as pressure, tapping or tickling, applied at any point over a considerable area of the body, evoked the response. Chemical reagents, like a drop of 50% alcohol, placed in the path of the worm, were also effective. An interesting special event which may cause the arrest or disappearance of peristalsis is a loss of contact between the ventral surface of the head region of the worm and the substratum.

A clean glass plate was covered with damp filter paper and supported in the air horizontally on a central pillar, so that it overhung the pillar on all sides. Five normal, vigorous earthworms were selected. Each in turn was placed upon the plate and allowed to crawl at random. Each crawled with continuous, regular peristaltic waves until it reached the edge of the plate and began to crawl over. There was now no surface, except that on which the worm lay, which the head could reach. In every test made the peristaltic waves beginning at the head were, in this situation, arrested or died out. In most cases the worm did not fall off the plate : sometimes it retreated a few centimetres by anti-peristalsis. Each worm was tested thus five times: in twenty out of the twenty-five tests the worm stopped crawling sufficiently early not to fall off. In each of these twenty tests where the worm did not fall off, a vertical glass plate was brought up and held in contact with the ventral surface of the head region of the worm. In eighteen out of the twenty cases in which this was done, the worm proceeded immediately to crawl down the vertical surface, and eventually fell. The results of this experiment are summarized in Table I.

Table I.
graphic
graphic

From many observations of a similar type to those recorded in the table it was concluded that a worm, if sufficiently excited by mechanical stimuli, would ignore the loss of contact of the head region with the substratum, but that a worm in a less excited condition regularly responded to it. There is a good deal of variation in readiness of response to the loss of contact in different individuals.

A vital link in the above reflex is provided by the supra-oesophageal ganglion. The paired supra-oesophageal ganglion was removed from each of the five earth-worms used in the previous experiment. Fifteen hours later all were healthy and crawled efficiently. Each was then subject to the same five tests as before. In all of the twenty-five tests the worms crawled unhesitatingly over the edge and fell. This result was confirmed by fifteen tests on a further three wórms, from which the supra-oesophageal ganglion had been extirpated.1 Some parallel may perhaps be drawn between the role of the supra-oesophageal ganglion in the suppression of crawling in these particular circumstances and the role of the same ganglion in the Arthropoda. Cutting through the circum-oesophageal commissures in an insect or a crab is followed by a marked heightening and increased recklessness of the body’s reflex activities (von Buddenbrock, 1928). Nevertheless, in Lumbricus, the functions of suppressing or arresting peristalsis are not localized exclusively in the supra-oesophageal ganglion, for the arrest of the peristaltic wave in response to tickling with a paint-brush can readily be evoked in a piece of worm after the first ten or more segments have been cut off.

(4) Further properties of the reflex

From numerous observations it was found that the peristaltic wave, wherever it was travelling in the body, could be arrested by suitable stimuli. The regions sensitive to the mechanical stimuli which evoke the reflex, on the other hand, are localized. From a series of tests, carried out on eighteen worms, the following general rules, as to the effects of mechanical stimuli in different regions, were obtained :

  • Stimuli applied on the cephalic one-third of the body may arrest the travelling peristaltic wave, whether it, is cephalic to, or caudal to, the point of stimulus.

  • Stimuli applied caudal to the clitellum and cephalic to a point half-way between the ends of the body may arrest a peristaltic wave travelling at, or caudal to, the point of stimulus, but not one cephalic to this point.

  • Stimuli on the caudal half of the body do not arrest peristalsis, but they evoke its appearance at the head.

The boundaries of the areas given above vary slightly from one individual to another.

The arrest of peristalsis can be evoked in pieces of the earthworm, also, provided that the piece includes areas receptive to the stimulus. The response to a paint-brush stimulus does not depend on the presence of the head segments. On progressively cutting off more and more of the segments at the cephalic end of the body, a point is eventually reached when peristalsis can no longer be arrested by cephalically placed stimuli. From tests on eight worms, it was found that this point lay around the half-way line between the ends of the body. If a worm is cut in half, stimuli applied at the cephalic end of the caudal half will not arrest, but may evoke a peristaltic wave. The absence of the extreme caudal segments in a piece of worm does not modify the position of the boundary between the half of the body receptive to immobilizing stimuli and the half unreceptive to them.

The dependence of the reflex on the continuity of the nerve cord between point of stimulus and point of response shows that the reaction under discussion definitely involves the nervous system and is not a purely mechanical effect. In nine worms the nerve cord was transected immediately cephalic to the clitellum, or in a corresponding position. Eighteen hours later all were healthy and responsive to stimuli. In none of them could the common reaction of initiating anti-peristalsis at the tail be effected by stimuli applied to the head. Likewise, in repeated tests, it was found impossible in any of these worms to arrest a peristaltic wave, travelling caudal to the cut in the nerve cord, by stimuli applied at points cephalic to it.

This reflex is very similar to that just described. Text-fig. 4 shows an example of the typical reflex. The normal anti-peristaltic wave has passed the first and most caudal pair of fixed points (the distance between which is represented by curve A) before the stimulus becomes effective. In the region represented by curve B the wave is in its shortening phase when the stimulus takes effect, and a sharp immobilization occurs. In curve C the elongation wave is seen to be halted, while in the region represented by curve D no wave appears. Curve E indicates the distance between a pair of points at the head; here the previous anti-peristaltic wave which has by now arrived is not arrested by the stimulus. The locomotory wave retains its shape, after its arrest, just as in the previous reaction. It was not possible to examine whether any relaxation of the musculature occurs during the immobilization.

Text-fig. 4.

The immobilization of an anti-peristaltic wave by a stimulus in the caudal region of the body. The black block represents the duration of the stimulus.

Text-fig. 4.

The immobilization of an anti-peristaltic wave by a stimulus in the caudal region of the body. The black block represents the duration of the stimulus.

The arrest of the anti-peristaltic wave may be part of two series of events. Usually the stimulus causing the arrest also evokes a peristaltic wave at the head. This peristaltic wave engulfs, as it travels tailwards, the stationary anti-peristaltic wave. In some cases, however, the halted anti-peristaltic wave is obliterated by a wave of longitudinal muscular contraction.

The reflex at present under discussion, like the previous one, is evoked by both chemical and mechanical stimuli. But it was not possible, owing to the spontaneous occurrence of immobilization of the anti-peristaltic wave, to test whether the loss of contact with a substratum evoked the reflex. The arrest of the wave does not happen in all regions of the body. In no case was it observed that stimuli at the tail immobilized anti-peristalsis when the wave was travelling in the more cephalic one-third of the body. Nor is the reflex evoked by stimuli in any part of the body.Tests on fifteen worms showed that mechanical stimuli might immobilize anti-peristalsis only when applied in the caudal half of the body. If the worm is deprived of the most caudal third of its body, the reflex can still be evoked. If a worm is cut in half, it is difficult to induce the cephalic half to perform antiperistaltic movements. Consequently it is impossible to tell whether or no the arrest of anti-peristalsis could occur in the severed cephalic half of a worm. The removal of a dozen or so cephalic segments does not destroy the Capacity of a worm to carry out the reflex immobilization of anti-peristalsis.

That this is a genuine nervous response is shown by its dependence on the continuity of the nerve cord between the point of stimulus and the point where the wave is arrested. In ten earthworms the nerve cord Was transected five to ten segments cephalic to the tip of the tail. Twelve hours later nine were alive with all segments responsive on both sides of the cut. In eight of these it was possible to induce anti-peristalsis, starting at the first segment cephalic to the cut. In each of these the application of mechanical stimuli to the body wall immediately cephalic to the transection of the cord elicited the immobilization of anti-peristalsis. In none of these did stimuli on the five to ten segments caudal to the transection cause the arrest of the anti-peristaltic wave cephalic to the cut.

An earthworm rarely continues to crawl tail first for any length of time. The direction of movement is spontaneously reversed in the following manner: while a worm is crawling tail first, “searching” movements appear at the head and develop into a peristaltic wave. At the same time as the peristaltic wave develops, the anti-peristaltic wave slows up and stops altogether. In its course tailwards the new peristaltic wave engulfs the stationary anti-peristaltic wave. A typical case of the spontaneous immobilization of anti-peristalsis is shown in Text-fig. 5.

Text-fig. 5.

The spontaneous immobilization of an anti-peristaltic wave at the appearance of a new peristaltic wave. The black block represents the appearance of searching movements of the head and their development into a new peristaltic wave.

Text-fig. 5.

The spontaneous immobilization of an anti-peristaltic wave at the appearance of a new peristaltic wave. The black block represents the appearance of searching movements of the head and their development into a new peristaltic wave.

In order to test whether the spontaneous immobilization of anti-peristalsis regularly accompanied the development of a peristaltic wave, the following series of observations was made. Eight worms were selected, and each in turn was induced to crawl tail first in a vigorous way. While the worm was crawling it was kept under observation. After several anti-peristaltic waves had passed, one of the waves would come to a standstill ; each time the wave thus halted spontaneously, it was noted whether or no a peristaltic wave was developing at the head. Likewise, each time a peristaltic wave developed, it was noted whether or no the anti-peristaltic wave halted. In one case alone out of thirty-six observations of the arrest of the anti-peristaltic wave, did the wave halt without a peristaltic wave being at the time in course of appearing. In one case alone out of thirty-six observations of the development of a peristaltic wave, did this occur without the anti-peristaltic wave being immobilized. In this case the two waves appeared to fuse into one peristaltic wave. From these and many other observations, it can be concluded that, when a worm is crawling tail first, the anti-peristaltic wave can be spontaneously immobilized in association with the spontaneous appearance of a new peristaltic wave. In this description the term “spontaneous” has been used to indicate that these events occurred without the application of any external stimulus; the use of the term is not intended to imply anything more than this. It may be worth emphasizing that the spontaneous immobilization of the anti-peristaltic wave is part of a larger behaviour-pattern ; the fate of the arrested wave is almost invariably the same : it is incorporated into the new wave of peristalsis.

In the course of the above observations, it was noted that, quite frequently, small searching movements of the head appeared and disappeared without developing into a peristaltic wave and without arresting the anti-peristaltic wave. In three cases such temporary searching movements of the head were accompanied by a transient stoppage of the anti-peristaltic wave. In two rather different cases a squirming movement of the tail was seen to be suppressed by the development of a peristaltic wave at the head. It would seem that active movement at the head tends to suppress movement at the tail. Possibly the reverse also is true: that active movement at the tail tends to suppress movement at the head.

The act of behaviour under discussion is not dependent on the presence of either the head or the tail segments. It happens after the removal of either the cephalic one-third, or the caudal one-third of the body. Like the two reflexes, this act of behaviour does depend, however, on the continuity of the nerve cord. In nine worms the cord was transected immediately cephalic to the clitellum. Eighteen hours later it was possible to induce in each worm a peristaltic wave in the cephalic part, and an anti-peristaltic wave in the caudal part, simultaneously pulling in opposite directions. Von Holst has reported a similar observation.

In the living earthworm the mechanisms described must frequently be brought into play. An arrest of the locomotory wave is really part of a larger pattern of behaviour. The reflex arrest of peristalsis may be a unit in one of two different behaviour-patterns, which lead to avoiding an unsatisfactory cephalic situation, or to escape from an attack at the head. In one pattern the peristaltic wave is arrested, and the worm turns to one side and crawls head first in a new direction. In the second pattern, which results presumably from a stronger stimulus or a more responsive nervous state in the worm, the same stimulus both arrests the peristaltic wave and initiates an anti-peristaltic wave at the tail. The worm then escapes, crawling tail first. Where the stimulus is very sharp or the worm very responsive, both behaviour-patterns are replaced or modified by the rapid shortening of the whole body known as the rapid shortening reflex. This reflex may only be a prelude to the carrying out of one or other of the acts of behaviour described above.

The reflex arrest of anti-peristalsis plays a similar role in reversing the direction of movement from tail first to head first: the stimulus which arrests the antiperistaltic wave also evokes at the head a new peristaltic wave. The spontaneous immobilization of anti-peristalsis, again, plays a necessary part in the co-ordination of the reversal of the direction of movement.

The rapid shortening reflexes of the earthworm are well known. Sharp stimuli on any part of the body cause a rapid jerk of the whole, accompanied by erection of the setae. This is supposed to be due to a fast conduction of excitations backwards and forwards in the dorsal giant fibres, causing a contraction of the longitudinal muscles. Different authors give different values for the speed of conduction of the rapid shortening reflexes: the lowest value is that of 1·5 m. per sec., given by Bovard.

If the nerve cord of a worm is transected, it regenerates rapidly, and the first reactions are conducted over the cut 2 or 3 days after it was made. But the fibres carrying the different reactions regenerate at different rates, so that the through-conduction of one reaction appears before that of another. As a rule the earliest reaction to be conducted past the transection is the initiation of anti-peristalsis at the tail in response to stimuli at the head; the rapid shortening reflexes are the slowest to be regenerated; while the arrests of the locomotory waves occupy an intermediate position between these two. By observing earthworms whose transected nerve cords are regenerating, it is possible to distinguish the units of the behaviour-complex which have different conduction paths. A series of observations of this sort has shown that the reflex arrest of peristalsis is not conducted from head to tail in the same fibres as those bearing the rapid shortening reflex. It would appear also that the immobilization of an anti-peristaltic wave by the spontaneous appearance of a peristaltic wave is conducted in a path different from either of the above two reflexes. In eight cases, in which the cord was transected and allowed to regenerate, the conduction of the reflex arrest of peristalsis, and of the immobilization of anti-peristalsis by the spontaneous development of peristalsis, was re-established over the cut at least a day before the power to conduct the rapid shortening reflex tailwards over the cut was regained. In three of these cases the spontaneous immobilization of anti-peristalsis was conducted from head to tail a day before the conduction of the reflex arrest of peristalsis was restored. Table II gives a summary of each case. The second column, headed “Arrest of peristalsis”, gives the number of days after the cut was made that the reflex arrest of peristalsis was first conducted over the cut. The third column, under the head “Immobilization of anti-peristalsis”, gives the number of days when first this act was conducted past the cut. The fourth column, headed “Rapid shortening reflex”, gives the number of days after the operation when this reflex was first conducted past the cut.

Table II.
graphic
graphic

The evidence that the reflex inhibition of anti-peristalsis is conducted by a different path in the nerve cord from that carrying the rapid shortening reflex from tail to head depends at present upon the three cases listed in Table III. Results of an experiment of the same nature as that described above are set out in Table III in the same way as in Table II. It will be seen that the reflex arrest of anti-peristalsis was re-established over the cut from i to 3 days before the rapid shortening reflex.

Table III.
graphic
graphic

Since the reflex arrest of anti-peristalsis is evoked by stimuli in the very region where stimuli fail to evoke the reflex arrest of peristalsis, the sensory elements of these two reflexes may be supposed to be distinct. There is evidence that all three acts of behaviour are conducted in different paths in the cord. In the first place, fibres conducting the reflex arrest of anti-peristalsis must be different from the fibres carrying the other two immobilizations, since they run from tail to head and since none of these fibres can be identified with the dorsal giant fibres, which are not polarized (Eccles, Granit & Young, 1932). The regeneration experiment cited in the last section has indicated a distinction between the path of the immobilization of anti-peristalsis by a peristaltic wave, and the path of the reflex arrest of peristalsis. In three worms the immobilization of anti-peristalsis was through-conducted a day before the other reaction. The musculature involved in the locomotor waves is in both cases the same. It may be, therefore, that some or all of these acts of behaviour have a final path in common. But at present there is little evidence as to the mode by which any immobilization takes place.

Three clear-cut acts of behaviour, definitely depending on the continuity of the ventral nerve cord, are under discussion. Disregarding, for the moment, the spontaneous immobilization of anti-peristalsis, the remaining two can be said to result regularly from certain types of external stimuli. It is therefore justifiable to call them reflexes, without committing ourselves as to their exact nature. The spontaneous immobilization of anti-peristalsis might be regarded as a response to stimuli engendered within the body of a worm by the movements of peristalsis; or it might be regarded as caused by some activity within the ganglia of the cephalic region.

If a walking man suddenly stops dead in his tracks, he maintains for a finite period one of the postures through which he passes during locomotion. This “freezing” of movement into posture in man is comparable to the immobilization of the travelling locomotory wave in the earthworm. Little can be said of the mechanism in Lumbricus, but it may be conjectured that this is essentially a central nervous phenomenon. Though at this stage there is insufficient evidence on which to base an hypothesis, any explanation put forward in the future will have to account for the quantitative gradations possible in the arrest. A locomotor wave may be merely slowed down ; it may be brought to a halt for a fraction of a second ; or it may be arrested indefinitely.

It has been argued that, in an arrest, both circular and longitudinal muscles might contract simultaneously and with equal force, with the consequence that, being mechanical antagonists, they exactly neutralize one another. This explanation is improbable. Von Holst showed that, in the rapid shortening reflex, both muscle sets contract, but that the longitudinal musculature has the greater mechanical effect when the body is in an extended condition, and hence the body shortens. Since in this case the contraction of the two muscle sets has an unequal result, it would be very difficult to imagine a mechanism so nicely balanced that, on both muscle sets contracting, neither the elongation phase, nor the shortening phase of the wave was disturbed.

I wish to express my gratitude to Prof. J. Gray, F.R.S., under whose supervision this work was done in Cambridge, and to Prof. T. T. Flynn, who supervised that part of the work carried out in Belfast. I am also greatly indebted to Dr C. F. A. Pantin, F.R.S., and to Prof. Henry Barcroft for their valuable advice.

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Plate I

Fig. 1. The arrest of a peristaltic wave by a stimulus at the head. This is one exposure from the film plotted in Fig. 2, and the distances A, B, C, D and E correspond to the curves in the figure.

Fig. 2. The arrest of an anti-peristaltic wave by a stimulus at the tail. The distances A, B, C, D and E correspond to the curves plotted in Text-fig. 4.

Fig. 3. The arrest of an anti-peristaltic wave by the spontaneous development of a peristaltic wave at the cephalic end (H). This exposure is taken from a film which is not plotted.

Plate I

Fig. 1. The arrest of a peristaltic wave by a stimulus at the head. This is one exposure from the film plotted in Fig. 2, and the distances A, B, C, D and E correspond to the curves in the figure.

Fig. 2. The arrest of an anti-peristaltic wave by a stimulus at the tail. The distances A, B, C, D and E correspond to the curves plotted in Text-fig. 4.

Fig. 3. The arrest of an anti-peristaltic wave by the spontaneous development of a peristaltic wave at the cephalic end (H). This exposure is taken from a film which is not plotted.

1

Recent observations of Gray and Lissmann (1938) clarify the factors involved in this situation. The fact that a worm, with a supra-oesophageal ganglion removed, continues to crawl when the cephalic half is suspended freely in air, would appear to be due to the release of reflex responses to the tension produced by its own weight. An intact worm suspended vertically in the air does not carry out rhythmic peristalsis, whereas a decapitated worm, in the same position, does carry out rhythmic peristaltic movements. This rhythm is abolished if the tension is reduced by suspending the decapitated worm in water. It would seem, therefore, that the supra-oesophageal ganglion, while permitting peristaltic movement in the worm lying on the substratum, prevents the evocation of peristaltic movements in response to tension, if the skin in the cephalic region of the body is not being stimulated by contact with another surface.