the immobilizatio of locomotorn y movements...

339

THE IMMOBILIZATION OF LOCOMOTORYMOVEMENTS IN THE EARTHWORM,

LUMBRICUS TERRESTRIS

BY H. O. J. COLLIERMusgrave Research Student in Zoology at Queen's University, Belfast

From the Sub-Department of Experimental Zoology, Cambridge, and theDepartment of Zoology, Queen's University, Belfast

(Received 12 October 1937)

(With One Plate and Five Text-figures)

LOCOMOTION AND THE ARREST OF LOCOMOTION

IN the earthworm, locomotion is effected by a slowly travelling wave of thinningand elongation, followed by a wave of thickening of the body. This is generallydescribed as a peristaltic wave. At any one moment, a whole peristaltic wave doesnot involve more than a part of the body of the worm. The thinning phase of thewave is produced by a local contraction of the circular musculature of the bodywall; a contraction which travels along the body from head to tail at a rate ofbetween 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 musculatureof the body wall, travelling at about the same rate. The whole movement hasrecently been analysed by Gray and Lissmann (1938). The worm is capable ofcrawling backwards by means of a movement of the same type, the wave travellingin the reverse direction, and usually described as anti-peristalsis.

The time taken for a peristaltic wave to pass along the whole body is from about3 to 7 sec. A worm presented with a noxious stimulus at the head, soon after aperistaltic wave has begun, would continue to crawl for some seconds subsequentlytowards the point of danger, were it not provided with a nervous mechanismarresting the movement of the peristaltic wave, and with mechanisms effecting itsescape. Three types of immobilization of the locomotory movements (two of whichfor reasons given later have been called reflexes), occur as part of the natural be-haviour of the worm. In the following description of them and in subsequentsections 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 segmentsrunning from the prostomium to the last segment of the clitellum are referred to asthe "cephalic one-third" of the body, and so on.

34° H. O. J. COLLIER

( I ) The reflex arrest of a peristaltic wave

When a worm is crawling head first, the application of mechanical or chemicalstimuli to the cephalic one-third of the body may result in an immobilization ofthe peristaltic wave, which is travelling tailwards. This immobilization, occurringabout 0-5 sec. after application of the stimulus, results from a halting of the thinningand thickening phases of the wave, wherever they are travelling in the body, withoutthe characteristic shape of the peristaltic wave disappearing. There are four possiblefutures for the halted peristaltic wave: (i) In certain circumstances it may, afteran indefinite period, travel on again towards the tail; (ii) It may remain halteduntil engulfed in a new peristaltic wave travelling down from the head; (iii) It maybe obliterated by the progression tailwards of the thickening phase of the wavealone; (iv) A thickening wave may appear at the caudal end of the thinningphase of the halted wave, this new wave of contraction travelling along the bodytowards 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 bodymay bring the anti-peristaltic wave to a halt, after an interval of about 0-4 sec, ina way similar to that described above. This arrest can take place at a considerabledistance from the point of stimulation, but it has not been observed to take effect onthe anti-peristaltic wave while the latter is travelling in the extreme cephalic region ofthe body. This response is normally accompanied by the appearance of a peristalticwave at the head, which engulfs, on its course to the tail, the immobilized anti-peristaltic 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 haltspontaneously. This halt is associated nearly always with the synchronous develop-ment of a peristaltic wave at the head. The immobilized wave is subsequentlyengulfed by the new peristaltic wave as it travels tailwards.

HISTORY

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

Locomotory Movements in the Earthworm, Lumbricus terrestris 341

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

"The hypothesis is made, that in each ganglion there is an 'inhibitorycentre'... .This 'inhibitory centre' is excited through the sensory endings of theskin (and often also of the musculature). If a segment is actively or passively madethinner, there occurs a specific reflex, evoked by the stimulus of thinning, in whichthe excitation caused by the stimulus flows into the next ganglion behind, and thereopposes the effect of the inhibitory stimuli. The action of the 'inhibitory centre' isstopped, and the inhibition is extinguished: in short, the inhibition is inhibited.... Ineach ganglion there occurs, after the extinction of the inhibition, the same rhyth-mical event—first the contraction of the circular musculature, then the contractionof the longitudinal musculature."

The above is a free translation of the passage (pp. 572-3) in which von Hoistadvances his hypothesis. He bases his assumption on a number of experiments.He found that the rate at which excitation of a peristaltic movement was conductedalong the nerve cord was considerably greater than normal in a length of cordwhich had been separated from the body wall by cutting the lateral nerves. Hereports that, if a part of the body is stretched artificially, the peristaltic wave traversesthat area more rapidly than is normal. If, on the other hand, a length of the bodyis prevented as nearly as possible from moving; the peristaltic wave is not con-ducted past it. Von Hoist also reports that the waves of thinning and thickeningtravel 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" thanon any other part of the ganglion. Von Hoist's interpretation is admittedly specu-lative ; the present state of our knowledge of the central nervous system of Lumbricusdoes not allow an exact description of behaviour in the terms of nerve physiology.

Interesting and suggestive as his views and experiments are, von Hoist'shypothesis of "inhibitory centres" does not directly concern the present account,in which the existence of definite mechanisms that immobilize the locomotorymovements is reported, without an attempt being made at present to explain themin the terms of nerve physiology.

In the above-mentioned paper the author describes two cases of the arrest of aperistaltic, wave at a point distant from a stimulus. If the cephalic region of a largepiece of worm is stretched, a peristaltic wave travelling away from the stretched areamay 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 areprobably particular cases of the responses described in this account; but, owing tothe difference in the nature of the stimuli, it is not easy to compare them to any oneof the reactions here described.

342 H. O. J. COLLIER

MATERIAL AND METHODS

The earthworm, Lumbricus terrestris, was the subject of these experiments.Where observations were made with the naked eye, the findings were confirmedupon a number of worms, kept in as nearly as possible the same external condi-tions. The main records were made with the cinematograph. Here I am whollyindebted 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 in2 cm. squares. Cinematograph films of the acts of behaviour were taken at afrequency of twenty exposures per sec. The speed of the camera was checkedby the use of a time-marker in the picture. Stimulation was effected either by thehandle or the brush of a paint-brush. The negative films were interpreted in thefollowing manner. A series of photographs showing the required reaction wasselected. Beginning at the first exposure of the series, the negative was projectedon to a sheet of white paper by means of an enlarger. The fixed points on the worm'ssurface, denoted by the borders of the white stripes that had been painted on it(see PI. I, figs, i, 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 requiredwas projected, the paper was moved slightly, and the same fixed points againrecorded 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, wasrecorded. The resulting chart gave the position of a series of fixed points on theworm 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 involveup 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, ineach enlargement on the chart. A series of curves, one for each of the enlargeddistances A, B, C, D, E, F, etc. was then plotted on the same time-scale, one curveabove the other (see Text-figs. 3, 4, 5). In all cases the wave of movement reachespoint 1 first and travels towards points 2-7. Thus the distance A increases as thethinning phase of peristalsis, or anti-peristalsis, approaches point 2. The distance Bthen begins to increase, as the thinning phase of the wave passes point 2 on itsway 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. Sub-sequently the distance B decreases likewise, and so on with C, D, etc. The curveproduced for each distance consists, therefore, of a flat base-line, which ascendsand falls at regular intervals as each fresh peristaltic or anti-peristaltic wave gripsand 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 curvefor the arrest of peristalsis was superimposed upon the curve for a normal peristalticwave, filmed immediately before. The peristaltic immobilization, which is less


sharp than the anti-peristaltic, was brought out by this means. Detailed accountsof each act of behaviour follow.

REFLEX ARREST OF PERISTALSIS

(1) The typical reflex

The longitudinal and circular musculature of the body wall are mechanicallyantagonistic. The lengthening phase of the peristaltic wave is due to contraction ofthe circular musculature of the body wall; while the shortening phase is accom-panied by relaxation of the circular musculature. A longitudinal slit cut in thedorsal body wall may be seen to open during the lengthening phase, in spite of thedecreased diameter of the body, and to close during the shortening phase, althoughthe body increases in diameter (Garrey & Moore, 1915). The shortening phaseof the peristaltic wave is brought about by a contraction of the longitudinal muscu-lature. A relaxation of the longitudinal musculature, unaccompanied by anappreciable change in shape of the body, follows shortly after the shortening hasbeen effected. This can be seen by observing a transverse slit cut in the dorsal bodywall: the slit may be seen to open during the elongation, and to remain open duringthe shortening phase of peristalsis; soon after the shortening phase is over, thetransverse slit closes, while the contours of the body remain the same, thus in-dicating a relaxation of the longitudinal muscles without a change in shape of theshortened body.

If two marks are made on the body surface, an increase in the distance betweenthem will indicate (where there is no passive stretch) a contraction of the circularmusculature. A decrease in the distance between them will indicate a contractionof the longitudinal muscles. The passage of a series of peristaltic waves will, there-fore, 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 offixed points are given. These figures illustrate two cases where the changes indistance between pairs of fixed points on the earthworm's surface during a normalperistaltic wave can be compared with those occurring when the head of the wormis stroked with a paint-brush. In the latter case, the peristaltic wave is seen tobe 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 thestimulus, and indicated in the figures by the lines of triangles. In Text-fig. 1 itwill be seen that the increase in length of the region where the shortening phase isoccurring (curves B and C) is abruptly stopped 0-4 sec. after the application of thebrush. The elongation phase (curve E) comes to an abrupt end 0-55 sec. afterapplication of the stimulus. The normal, full contraction is completed in neitherphase of the peristaltic wave; while, in that region where the elongation is at itsheight (curve D), no normal shortening sets in. Curve A, however, gives themovements of a part of the body in which the wave has completed both phases inits cycle before the stimulus takes effect. In short, the result of a paint-brush stimulusat 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 astimulus at the tail caused a general shortening of the body. The immobilization

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•Text-fig. 1. The immobilization of a peristaltic wave in response to a stimulus in the head region ofthe body. A A A = normal wave. ••• = arrested wave. The black block gives the duration of thestimulus.

response, which I have called the reflex arrest of peristalsis, can be evoked regularlyin normal, fresh earthworms.

Though the photographic record shows that both phases of the peristaltic waveare immobilized without the posture being lost, it is not possible to decide from such

Locomotory Movements in the Earthworm, Lumbncus terrestris 345

records what is the mechanism of the arrest, or the actual state of contraction of themuscles during the immobilization. The mechanism of the arrest will be discussedlater. There is some, but not much, evidence to suggest that the muscles actuallyrelax, at least partially, during the arrest, but that the posture is not lost becausethere are not strong enough forces tending to destroy it. A low-power microscopicexamination of the films, using a ruled eyepiece, reveals that after normal reflexarrests there may be an increase in breadth of up to 10% in the region of the

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elongation. There is a corresponding, though smaller, decrease in length of up to5 % in this region. A different series of observations suggests that there may be, inthe immobilization, an actual relaxation of the circular musculature, without anymarked change in shape of the elongated region. Dorsal longitudinal slits, about2-3 mm. in length, were made in the body wall of ten worms. In each worm the

JBB-xviii 23


observation of Garrey & Moore, that the slit widened during the elongation phaseof peristalsis, was confirmed. In each, a peristaltic wave was then arrested, by anappropriate stimulus in the head region, while the elongation involved the area ofthe slit. Each time this was done, the slit could be seen to close, either wholly orpartially, without the general shape of the stationary wave being lost. It was notfound practicable to carry out a similar series of observations on the longitudinalmusculature..

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Text-fig. 3. A fresh peristaltic wave merging with a previously immobilized wave. The black blockrepresents the duration of the inhibitory stimulus; the vertical column represents an interval of4 sec. without movement.

(2) Events following the reflex arrest

Several different events may follow the arrest of the peristaltic wave. Which ofthem actually occurs may be determined by such factors as the strength, or the typeof the original stimulus, or by the state of the earthworm. In some cases the waveis only arrested momentarily. Text-fig. 2 illustrates such a case, when, after a lightstimulus, the wave is arrested for a brief period and then continues its course. Inother cases the wave may be arrested and remain stationary for 3 or 4 sec. beforeit 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 wavemay 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 bearrested, the longitudinal musculature continues to contract, and obliterates theperistaltic wave. Observation and the analysis of film records show that thecontinuing wave of longitudinal muscular contraction may run caudalwards, or itmay appear at the caudal end of the elongated area and run towards the head.

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

Mechanical stimuli, such as pressure, tapping or tickling, applied at any pointover a considerable area of the body, evoked the response. Chemical reagents, likea drop of 50 % alcohol, placed in the path of the worm, were also effective. Aninteresting special event which may cause the arrest or disappearance of peri-stalsis is a loss of contact between the ventral surface of the head region of the wormand the substratum.

A clean glass plate was covered with damp filter paper and supported in the airhorizontally on a central pillar, so that it overhung the pillar on all sides. Fivenormal, vigorous earthworms were selected. Each in turn was placed upon theplate and allowed to crawl at random. Each crawled with continuous, regularperistaltic 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 headcould 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 offthe plate: sometimes it retreated a few centimetres by anti-peristalsis. Each wormwas tested thus five times: in twenty out of the twenty-five tests the wormstopped crawling sufficiently early not to fall off. In each of these twenty testswhere the' worm did not fall off, a vertical glass plate was brought up and held incontact with the ventral surface of the head region of the worm. In eighteen out ofthe twenty cases in which this was done, the worm proceeded immediately to crawldown the vertical surface, and eventually fell. The results of this experiment aresummarized in Table I.

Table I

Earthworm

12

345

Total

No. of tests

5S555

25

Cases inwhich crawling

stopped

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Cases inwhich theworm did

not fall

52

355

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Cases in whichthe worm, nothaving fallen,

proceeded to crawldown a vertical

surface

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From many observations of a similar type to those recorded in the table it wasconcluded that a worm, if sufficiently excited by mechanical stimuli, would ignorethe loss of contact of the head region with the substratum, but that a worm in a

23-2


less excited condition regularly responded to it. There is a good deal of variation inreadiness 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 andcrawled efficiently. Each was then subject to the same five tests as before. In all ofthe twenty-five tests the worms crawled unhesitatingly over the edge and fell. Thisresult was confirmed by fifteen tests on a further three w6rms, from which thesupra-oesophageal ganglion had been extirpated.1 Some parallel may perhaps bedrawn between the role of the supra-oesophageal ganglion in the suppression ofcrawling in these particular circumstances and the role of the same ganglion in theArthropoda. Cutting through the circum-oesophageal commissures in an insect ora crab is followed by a marked heightening and increased recklessness of the body'sreflex activities (von Buddenbrock, 1928). Nevertheless, in Lumbricus, the func-tions of suppressing or arresting peristalsis are not localized exclusively in thesupra-oesophageal ganglion, for the arrest of the peristaltic wave in response totickling with a paint-brush can readily be evoked in a piece of worm after the firstten or more segments have been cut off.

(4) Further properties of the reflex

From numerous observations it was found that the peristaltic wave, wherever itwas travelling in the body, could be arrested by suitable stimuli. The regionssensitive to the mechanical stimuli which evoke the reflex, on the other hand, arelocalized. From a series of tests, carried out on eighteen worms, the followinggeneral rules, as to the effects of mechanical stimuli in different regions, wereobtained:

(i) Stimuli applied on the cephalic one-third of the body may arrest thetravelling peristaltic wave, whether it is cephalic to, or caudal to, the point ofstimulus.

(ii) Stimuli applied caudal to the clitellum and cephalic to a point half-waybetween 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.

(iii) Stimuli on the caudal half of the body do not arrest peristalsis, but theyevoke its appearance at the head.

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

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 thecephalic half is suspended freely in air, would appear to be due to the release of reflex responses tothe tension produced by its own weight. An intact worm suspended vertically in the air does notcarry out rhythmic peristalsis, whereaB a decapitated worm, in the same position, does carry outrhythmic peristaltic movements. This rhythm is abolished if the tension is reduced by suspendingthe decapitated worm in water. It would seem, therefore, that the supra-oesophageal ganglion, whilepermitting peristaltic movement in the worm lying on the substratum, prevents the evocation ofperistaltic movements in response to tension, if the skin in the cephalic region of the body is notbeing stimulated by contact with another surface.


The arrest of peristalsis can be evoked in pieces of the earthworm, also, providedthat 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 pro-gressively 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 cephali-cally placed stimuli. From tests on eight worms, it was found that this point layaround 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 evokea peristaltic wave. The absence of the extreme caudal segments in a piece of wormdoes not modify the position of the boundary between the half of the body receptiveto immobilizing stimuli and the half unreceptive to them.

The dependence of the reflex on the continuity of the nerve cord between pointof stimulus and point of response shows that the reaction under discussion de-finitely involves the nervous system and is not a purely mechanical effect. In nineworms the nerve cord was transected immediately cephalic to the clitellum, or ina corresponding position. Eighteen hours later all were healthy and responsive tostimuli. In none of them could the common reaction of initiating antiTperistalsisat 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, travellingcaudal to the cut in the nerve cord, by stimuli applied at points cephalic to it.

REFLEX ARREST OF ANTI-PERISTALSISThis 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 mostcaudal 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 thewave is in its shortening phase when the stimulus takes effect, and a sharp im-mobilization occurs. In curve C the elongation wave is seen to be halted, while inthe region represented by curve D no wave appears. Curve E indicates the distancebetween a pair of points at the head; here the previous anti-peristaltic wave whichhas by now arrived is not arrested by the stimulus. The locomotory wave retains itsshape, after its arrest, just as in the previous reaction. It was not possible toexamine whether any relaxation of the musculature occurs during the immo-bilization.

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-peristalticwave. In some cases, however, the halted anti-peristaltic wave is obliterated by awave of longitudinal muscular contraction.

The reflex at present under discussion, like the previous one, is evoked by bothchemical and mechanical stimuli. But it was not possible, owing to the spon-taneous occurrence of immobilization of the anti-peristaltic wave, to test whetherthe loss of contact with a substratum evoked the reflex. The arrest of the wave doesnot happen in all regions of the body. In no case was it observed that stimuli at

35° H. O. J. COLLIER

the tail immobilized anti-peristalsis when the wave was travelling in the morecephalic one-third of the body. Nor is the reflex evoked by stimuli in any part ofthe body.* Tests on fifteen worms showed that mechanical stimuli might immobilizeanti-peristalsis only when applied in the caudal half of the body. If the worm isdeprived of the most caudal third of its body, the reflex can still be evoked. If aworm is cut in half, it is difficult to induce the cephalic half to perform anti-peristaltic movements. Consequently it is impossible to tell whether or no the

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Text-fig. 4. The immobilization of an anti-peristaltic wave by a stimulus in the caudal regionof the body. The black block represents the duration of the stimulus.

arrest of anti-peristalsis could occur in the severed cephalic half of a worm. Theremoval of a dozen or so cephalic segments does not destroy the Capacity of aworm to carry out the reflex immobilization of anti-peristalsis.

That this is a genuine nervous response is shown by its dependence on the con-tinuity of the nerve cord between the point of stimulus and the point where the waveis arrested. In ten earthworms the nerve cord Was transected five to ten segmentscephalic to the tip of the tail. Twelve hours later nine were alive with all segmentsresponsive 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 thesethe application of mechanical stimuli to the body wall immediately cephalic to thetransection of the cord elicited the immobilization of anti-peristalsis. In none ofthese did stimuli on the five to ten segments caudal to the transection cause thearrest of the anti-peristaltic wave cephalic to the cut.

SPONTANEOUS IMMOBILIZATION OF ANTI-PERISTALSISAn earthworm rarely continues to crawl tail first for any length of time. The

direction of movement is spontaneously reversed in the following manner: whilea worm is crawling tail first, "searching" movements appear at the head and

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Text-fig. 5: The spontaneous immobilization of an anti-peristaltic wave at the appearance of a newperistaltic wave. The black block represents the appearance of searching movements of the headand their development into a new peristaltic wave.

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 thenew peristaltic wave engulfs the stationary anti-peristaltic wave. A typical case ofthe spontaneous immobilization of anti-peristalsis is shown in Text-fig. 5.

In order to test whether the spontaneous immobilization of anti-peristalsisregularly accompanied the development of a peristaltic wave, the following seriesof observations was made. Eight worms were selected, and each in turn wasinduced to crawl tail first in a vigorous way. While the worm was crawling it waskept under observation. After'several anti-peristaltic waves had passed, one of the

352 H. 0. J. COLLIER

waves would come to a standstill; each time the wave thus halted spontaneously, itwas 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-peristalticwave halted. In one case alone out of thirty-six observations of the arrest of theanti-peristaltic wave, did the wave halt without a peristaltic wave being at the timein course of appearing. In one case alone out of thirty-six observations of thedevelopment of a peristaltic wave, did this occur without the anti-peristaltic wavebeing immobilized. In this case the two waves appeared to fuse into one peristalticwave. From these and many other observations, it can be concluded that, when aworm is crawling tail first, the anti-peristaltic wave can be spontaneously immo-bilized in association with the spontaneous appearance of a new peristaltic wave.In this description the term "spontaneous" has been used to indicate that theseevents occurred without the application of any external stimulus; the use of theterm is not intended to imply anything more than this. It may be worth emphasizingthat the spontaneous immobilization of the anti-peristaltic wave is part of a largerbehaviour-pattern; the fate of the arrested wave is almost invariably the same: it isincorporated 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 de-veloping into a peristaltic wave and without arresting the anti-peristaltic wave.In three cases such temporary searching movements of the head were accompaniedby a transient stoppage of the anti-peristaltic wave. In two rather different casesa squirming movement of the tail was seen to be suppressed by the development ofa peristaltic wave at the head. It would seem that active movement at the headtends to suppress movement at the tail. Possibly the reverse also is true: thatactive movement at the tail tends to suppress movement at the head.

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

THE ROLE OF THE LOCOMOTORY IMMOBILIZATIONSIN NORMAL BEHAVIOUR

In the living earthworm the mechanisms described must frequently be broughtinto play. An arrest of the locomotory wave is really part of a larger pattern ofbehaviour. The reflex arrest of peristalsis may be a unit in one of two differentbehaviour-patterns, which lead to avoiding an unsatisfactory cephalic situation, orto 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 thesecond pattern, which results presumably from a stronger stimulus or a more


responsive nervous state in the worm, the same stimulus both arrests the peristalticwave 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 thewhole body known as the rapid shortening reflex. This reflex may only be a preludeto 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 directionof movement from tail first to head first: the stimulus which arrests the anti-peristaltic wave also evokes at the head a new peristaltic wave. The spontaneousimmobilization of anti-peristalsis, again, plays a necessary part in the co-ordinationof the reversal of the direction of movement.

THE RELATIONS OF THE LOCOMOTORY IMMOBILIZATIONSTO THE RAPID SHORTENING REFLEXES

The rapid shortening reflexes of the earthworm are well known. Sharp stimulion any. part of the body cause a rapid jerk of the whole, accompanied by erection ofthe setae. This is supposed to be due to a fast conduction of excitations backwardsand forwards in the dorsal giant fibres, causing a contraction of the longitudinalmuscles. Different authors give different values for the speed of conduction of therapid shortening reflexes: the lowest value is that of 1-5 m. per sec, given byBovard.

If the nerve cord of a worm is transected, it regenerates rapidly, and the firstreactions are conducted over the cut 2 or 3 days after it was made. But the fibrescarrying the different reactions regenerate at different rates, so that the through-conduction of one reaction appears before that of another. As a rule the earliestreaction to be conducted past the transection is the initiation of anti-peristalsis atthe tail in response to stimuli at the head; the rapid shortening reflexes are theslowest to be regenerated; while the arrests of the locomotory waves occupy anintermediate position between these two. By observing earthworms whose tran-sected nerve cords are regenerating, it is possible to distinguish the units of thebehaviour-complex which have different conduction paths. A series of observationsof this sort has shown that the reflex arrest of peristalsis is not conducted fromhead to tail ir> the same fibres as those bearing the rapid shortening reflex. Itwould appear also that the immobilization of an anti-peristaltic wave by thespontaneous appearance of a peristaltic wave is conducted in a path different fromeither of the above two reflexes. In eight cases, in which the cord was transectedand allowed to regenerate, the conduction of the reflex arrest of peristalsis, and ofthe 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 rapidshortening reflex tailwards over the cut was regained. In three of these cases thespontaneous immobilization of anti-peristalsis was conducted from head to tail aday before the conduction of the reflex arrest of peristalsis was restored. Table IIgives 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 "Immobili-zation of anti-peristalsis", gives the number of days when first this act was con-ducted past the cut. The fourth column, headed "Rapid shortening reflex", givesthe number of days after the operation when this reflex was first conducted pastthe cut.

Table II

Earthworm

i

z34S678

/\rrest oiperistalsis

43344546

Immobilizationof anti-

peristalsis

33344445

Rapidshortening

reflex

67476

IO

5IO

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

Table III

Earthworm

12

3

Arrest ofanti-peristalsis

544

Rapidshortening

reflex

855

THE RELATIONS BETWEEN THE IMMOBILIZATIONSSince 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 ofthese two reflexes may be supposed to be distinct. There is evidence that all threeacts 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 thefibres carrying the other two immobilizations, since they run from tail to head andsince none of these fibres can be identified with the dorsal giant fibres, which arenot polarized (Eccles, Granit & Young, 1932). The regeneration experiment citedin the last section has indicated a distinction between the path of the immobilizationof anti-peristalsis by a peristaltic wave, and the path of the reflex arrest of peristalsis.In three worms the immobilization of an ti-peristalsis was through-conducted a daybefore the other reaction. The musculature involved in the locomotor waves is inboth 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 modeby which any immobilization takes place.

THE NATURE OF THE IMMOBILIZATIONSThree clear-cut acts of behaviour, definitely depending on the continuity of

the ventral nerve cord, are under discussion. Disregarding, for the moment, thespontaneous immobilization of anti-peristalsis, the remaining two can be said toresult regularly from certain types of external stimuli. It is therefore justifiable tocall them reflexes, without committing ourselves as to their exact nature. Thespontaneous immobilization of anti-peristalsis might be regarded as a response tostimuli 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 cephalicregion.

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

It has been argued that, in an arrest, both circular and longitudinal musclesmight contract simultaneously and with equal force, with the consequence that,being mechanical antagonists, they exactly neutralize one another. This explanationis improbable. Von Hoist showed that, in the rapid shortening reflex, both musclesets contract, but that the longitudinal musculature has the greater mechanicaleffect 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, itwould be very difficult to imagine a mechanism so nicely balanced that, on bothmuscle sets contracting, neither the elongation phase, nor the shortening phase ofthe wave was disturbed.

SUMMARY1. 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 about0-5 sec, if the nearest part of the wave is 5 cm. from the point of stimulus. Thisresponse is of regular occurrence, and it depends on the continuity of the nervecord between the point of stimulus and the region of the wave. It is thereforenamed the reflex arrest of peristalsis.

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


3. The receptors of the reflex lie on the cephalic half of the body. Stimuliapplied on the most cephalic one-third of the body may arrest a peristaltic wavecephalic 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 inthe head region. In this last case the reflex depends upon the presence of the supra-oesophageal ganglion. The response to mechanical stimuli, however, dependsneither on the presence of the cephalic one-third of the body, nor on the presence ofthe tail segments.

5. A similar reflex arrest of anti-peristalsis occurs in response to mechanical orchemical stimuli on the caudal half of the body. The time interval between stimulusand response at 5 cm. from the point of stimulus is about 0-4 sec. The anti-peri-staltic wave was not observed to be arrested while travelling in the most cephalicone-third of the body.

6. The arrest of the anti-peristaltic wave is due, too, to a cessation of movementof 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 nervepaths from them run in both directions. The reflex does not depend on the presenceof either the head or the tail segments. It can be obtained in a worm with the mostcaudal 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 peristalticwave can be observed in the spontaneous reversal of the direction of crawling. Thisact of behaviour, which is named the spontaneous immobilization of anti-peristalsis,does not depend on the presence of either the most cephalic one-third or the mostcaudal one-third of the body. Though this act of. behaviour need not be consideredas a reflex, its performance depends on the continuity of the nerve cord between thenew peristaltic wave and the anti-peristaltic wave that is immobilized.

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

10. There is little evidence to throw light on the mode of action of these threeimmobilizations. They may be compared to the "freezing" of movement intoposture found in insects and vertebrates. It is to be expected that their mechanismwill prove to lie within the central nervous system.

I wish to express my gratitude to Prof. J. Gray, F.R.S., under whose supervisionthis work was done in Cambridge, and to Prof. T. T. Flynn, who supervised thatpart 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.

JOURNAL OF EXPERIMENTAL BIOLOGY, XV, 3. PLATE 1

60

COLLIER.—THE IMMOBILIZATION OF LOCOMOTORY MOVEMENTS IN THEEARTHWORM, LUMBRICUS TERRESTRIS (pp. 339—357).


REFERENCES

BOVARD, J. F. (1918). Univ. Calif. Publ. Zool. 18, 103.BUDDENBROCK, W. VON (1928). Gruttdriit der vergleichenden Physiologte, pp. 237, 238.

Berlin: Borntraeger.ECCLES, J. C , GRANIT, R. & YOUNG, J. Z. (1932). J. Physiol. TT, 23 P.

GARREY, W. E. & MOORE, A. R. (1915). Amer. J. Physiol. 39, 139.

GRAY, J. & LISSMANN, H. W. O938). J. exp. Biol. 16 (in the Press).

HOLST, E. VON (1932). Zool. Jb. Abt. 3, 51, 547.

KNOWLTON, F. P. Si MOORE, A. R. (1917). Amer.J. Physiol. 44, 490.

EXPLANATION OF PLATE I

Fig. 1. The arrest of a peristaltic wave by a stimulus at the head. This is one exposure from thefilm 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, Dand 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 waveat the cephalic end (H). This exposure is taken from a film which is not plotted.

the immobilizatio of locomotorn y movements...

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