Forced Movements, Tropisms, and Animal Conduct

l/IKIIj li<rlrfr||rr Ifisiimtc i, IL MCIIIOAK, C**Itifnlik llftivcfiitf II. I V, ClhTKWlCIl/f^ IlirfiriJ Oaiversify By E. M. EAST and D. P. JONES, Bussey Institution, Harvard University EUctrotyPed and Printed hy J, B. Lippincoti Company The Washington Square Press^ Philadelphia, U.S.A. Tub rapidly incmiHiiig sppciaiixation makes it im- poKsiblu for one author Jo <'.ovor natisfactorily the whole field of modern Biology. Tiiis Hituation, which exists in all tile sciences, has induced FiHglish authors to issue series of rnonograiihs in Biocheinistry, Physiology, and Physics. A number of/Aineriiian biologists Imvi^ileidded to'jirovule the mum oiiporfunity for the study of Experimental Biology.

Biolog}% which not long ago was purely doscriptivo ami speculative, has lieguu to adopt the methods of the exact sciences, recognizing that for permanent progress not only exiMjriinents are required but that the experi¬ ments should bo of a quantitative character. It will be the pnrtRise tif this series of monographs to emphasize* and further as mueir as possible this development of Biology. Exporiimmtal Biology and tfeneral Physiology are one and the same science, by method as well as by contents, since both aim at explaining life from the physico-chemical constitution of living matter. The series of monographs on Exporiimmtal liiology will therefore include the Hold of traditional tleneral Physiology.

Animal conduct is known to many through the roman¬ tic tales of popularizers, through the descriptive work of biological observers, or through the attempts of vital- ists to show the inadequacy of physical laws for the explanation of life. Since none of these contributions are based upon quantitative experiments, they have led only to speculations, which are generally of an anthropo¬ morphic or of a purely verbalistic character. It is the aim of this monograph to show that the subject of ATiitYial conduct can be treated by the quantitative methods of the physicist, and that these methods lead to the forced movement or tropism theory of animal conduct, which was proposed by the writer thirty years ago, but which has only recently been carried to some degree of com¬ pletion. Many of the statements, especially those con¬ tained in the first four chapters of the book, are familiar to those who have read the writer’s former publications, but so much progress has been made in the last few years that a new and full presentation of the subject seemed desirable. Chapters V to XIII and Chapter XVI are partly or entirely based on new experiments.

Only that part of the literature has been considered which contributes to or prepares the way for quantitative experiments. The writer is under obligation for valuable criticism to Ms wife, to Professor T. H. Morgan, and to Lieutenant Leonard B. Loeb, who were kind enough toi read the manuscript. J. L. II. The Symmetry Relations of the Animal Body as the Start¬ ing Point for the Theory op Animal Conduct. 19 V. Heliotropism. The Influence of One Source of Light. .. 47

XL The Relative Heliotropic Efficiency of Light of Differ¬ ent Wave Lengths. 100 1. Forced Position of Larva of the Dragon Fly whose Left Cerebral 2. Forced Position of Shrimp when Galvanic Current Goes from Head 3. Forced Position of Shrimp when Positive Current Goes from Tail to 4. Position of Legs of Shrimp when Current Goes Sideways through the 5~6. Show Same Effects of Current on the Common Crawfish as Those 7. Diagram Indicating the Orientation of the Neurons for Flexor- and

8-9, Diagram Indicating Orientation of Neurons for Flexor and Extensor Muscles of Third and Fifth Pairs of Legs. 40 10. Forced Position of Amhlystoma Larva Under Influence of Galvanic 11. Forced Position of Amhlystoma Larva When Current Goes from Tail 12. Tentacles and Manubrium of Jellyfish Under Influence of Galvanic 13. Strip of Jellyfish Under Influence of Galvanic Current. 42 16. Showing that Positively Hehotropic Animals WiU Move from Sun- Kght into Shade if Illumination of Both Eyes Remains the Same.... 50

17. Position of Water Scorpion When Eight Eye is Towards the Light.. 53 18. Positions of Banatra When Light is in Front and Behind Animal.... 54 21. Position of Robber Fly when Lower Halves of Both Eyes are Blackened 57 22. Posation of Robber Fly when Upper Halves of Both Eyes are Blackened 58 23. Diagram Showing Position of the Flagellum as Seen in a Viscid 25. Same Animals After Position of Aquarium was Reversed. 64 26. Polyps of Eudendrium all Growing Towards Source of Light. 66

28. Diagram of Apparatus Used to Produce Differential Bilateral Light 30. Diagram for Constructing Direction of Motion of Larvae. 80 34. Method of Determining the Relative Heliotropic Efficiency of Two 35. Geotropic Curvature of Stems of BryophtjUum calycinum . 120 36. All Stems were Originally Straight and Suspended Horizontally. 121 37. When the Size of the Leaf is Reduced by Cutting Out Pieces from the 39. Influence of Motion of the Hand on a Swarm of Sticklebacks in an

40. The Regenerating Polyp of Tuhularia in Contact with Glass Wall of 42. Method of Proving the Pammceda are not Positive to Acid of Low The analysis of the mechanism of voluntary and instinctive actions of animals which we propose to under¬ take in this volume is based on the assumption that all these motions are determined by internal or external forces. Our task is facilitated by the fact that the over¬ whelming majority of organisms have a bilaterally sym¬ metrical structure, i.e., their body is like our own, divided into a right and left half.

The significance of this symmetrical structure lies in the fact that the morphological plane of symmetry of an animal is also its plane of symmetry in physiological or dynamical respect, inasmuch as under normal con¬ ditions the tension in symmetrical muscles is the same, and inasmuch as the chemical constitution and the velocity of chemical reactions are the same for symmetrical ele¬ ments of the surface of the body, e.g., the sense organs. Normally the processes inducing locomotion are equal in both halves of the central nervous system, and the ten¬ sion of the symmetrical muscles being equal, the animal moves in as straight a line as the imperfections of its

locoinotor apparatus permit. If, however, the velocity of chemioal reactions in one side of the body, e.g., in one eye of an insect, is increased, the physiological symmetry of both sides of the brain and as a consequence the equahty of tension of the symmetrical muscles no longer exist. The muscles connected with the more strongly illuminated eye are thrown into a stronger tension,®- and if now impulses for locomotion originate in the central nervous system, they will no longer produce an equal response in the symmetrical muscles, but a stronger one in the muscles turning the head and body of the animal to the source of light. The animal will thus be compelled to change the direction of its motion and to turn to the source of light. As soon as the plane of symmetry goes through the source of light, both eyes receive again equal illumination, the tension (or tonus) of symmetrical muscles becomes equal again, and the impulses for locomotion will now produce equal activity in the symmetrical muscles. As a conse¬ quence, the animal will move in a straight line to the source of light until some other asymmetrical disturbance once more changes the direction of motion.

"What has been stated for light holds true also if light is replaced by any other form of energy. Motions caused by light or other agencies appear to the layman as expres¬ sions of will and purpose on the part of the animal, whereas in reality the animal is forced to go where carried by its legs. For the conduct of animals consists of forced movements. The term forced movements is borrowed from brain physiology, where it designates the fact that certain ani¬ mals are no longer able to move in a straight line when

a We are speaking of positively heliotropic animals exposed to only certain parts of the brain are injured, but are compelled to deviate constantly toward one side, which is (accord¬ ing to the species and the location of the injury in the brain) either the side of the injury or the opposite side. The explanation of these forced movements is that on accormt of the one-sided injury of the brain the tension of the symmetrical muscles is no longer the same. As a consequence, the impulses' for locomotion which are equal for symmetrical muscles will cause greater contraction in certain muscles of one side of the body than in the symmetrical muscles of the other side, and the animal will no longer move in a straight line. The only difference between the forced movements induced by unequal illu¬ mination of the two eyes and by injury to the brain is that in the latter case the forced movements may last for days or throughout the whole life, while in the former case they last only as long as the iUumination on the two sides of the body is unequal. If we bring about a per¬ manent difference in illumination in the eyes, e.g., by blackening one eye in certain insects, we can also bring about permanent circus motions. This shows that animal conduct may be justly designated as consisting of forced movements.

The idea that the morphological and physiological symmetry conditions in an animal are the key to the understanding of animal conduct demanded that the same principle should explain the conduct of plants, since plants also possess a symmetrical structure. The writer was able to show that sessile animals behave toward light exactly as do sessile plants; and motile animals like motile plants. The forced orientations of plants by outside sources of energy had been called tropisms; and the theory of animal conduct based on the symmetrical stmc-

ture of tlieir body was, therefore, designated as the tropism theory of animal conduct. We started with symmetrical animals since in their case the analysis of conduct is comparatively simple; the results obtained in the study of these symmetrical organisms allow us also to understand the conduct of asymmetrical animals. We shall see that the principles underlying their conduct are the same as in the case of symmetrical animals, the asymmetry of the body altering only the geometrical character of the path in which the animal is compelled to move, not, however, the mechanism of conduct. While a perfectly symmetrical organism, possessed of positive heliotropism, moves in a straight line to the source of light, the path deviates from the straight line in the case of an asymmetrical organism and may in some cases, as, e.g., in Euglena, be a spiral around the straight line as an axis. Some authors have tried to use asymmetrical organisms as a starting point for the analysis of conduct, but since it is impossible to understand the conduct of the asymmetrical organisms unless it is based upon that of the symmetrical animals, these authors have been led to anthropomorphic specula¬ tions, such as “selection of random movements” which, as far as the writer can see, cannot even be expressed in the language of the physicist.

Although the tropism theory of animal conduct was offered thirty years ago 285,286,287 acceptance was delayed by various circumstances. In the first place, the majority of the older generation of biologists did not realize that not only the methods of the physicist are needed but also the physicist’s general viewpoint con¬ cerning the nature of scientific explanation. In many causes the problem of animal conduct is treated in a way wliich corresponds more to tlie viewpoint of the intro¬ spective psychologist than to that of the physicist. The attempts to explain animal conduct in terms of “trial and error” or of vague “physiological states” may serve as examples. None of these attempts have led or can lead to any exact quantitative experiments in the sense of the physicist. Other biologists have still more openly adopted an anthropomorphic method of explana¬ tion. If pleasure and pam or curiosity play a role in human conduct, why should it be otherwise in animal conduct? The answer to this objection is that typical forced movements when produced in human beings, as, e.g., in Meniere’s disease or when a galvanic current goes through the brain, are not accompanied by sensations of pleasure or pain, and there is no reason to attribute the circus movements of an animal, after lesion of the brain or when one eye is blackened, to curiosity or thrills of delight. An equally forcible answer lies in the fact that plants show the same tropisms as animals, and it seems somewhat arbitrary to assume that the bending of a plant to the window or the motion of swarmspores of algae to the window side of a vessel are accompanied or deter¬ mined by curiosity or by sensations of joy or satisfaction. And finally, since we know nothing of the sentiments and sensations of lower animals, and are still less able to meas¬ ure them, there is at present no place for them in science.

The second difficulty was created by the fact that the Aristotelian viewpoint still prevails to some extent in biology, namely, that an animal moves only for a pur¬ pose, either to seek food or to seek its mate or to under¬ take something else connected with the preservation of the individual or the race.'^ The Aristotelians had ex¬ plained the processes in the inanimate world in the same teleological way. Science began when G-alileo overthrew this Aristotelian mode of thought and introduced the method of quantitative experiments which leads to mathe¬ matical laws free from the metaphysical conception of purpose. The analysis of animal conduct only becomes scientific in so far as it drops the question of purpose and reduces the reactions of animals to quantitative laws. This has been attempted by the tropism theory of ani¬ mal conduct.

bThis view is still held, especially among authors, who lean more or less openly to vitalism, e.g., v. Uexkiill, Jordan, Franz, Bauer, Budden- brock, and others. The starting point for a scientific and quantitative analysis of animal conduct is the symmetry relations of the animal body. The existence of these symmetry i*ela- tions reduces the analysis to a comparatively simple problem. Organisms show two forms of symmetry, radial sym¬ metry, for which jellyfish and the stems and roots of most plants offer a well-known example, and lateral sym¬ metry, such as exists in man and most animals. In radial symmetry the peripheral elements are distributed equally about an axis of symmetry, in the case of lateral sym¬ metry the peripheral elements are distributed equally to the right and left of the plane of symmetry (or the median plane) by which the body is divided into a right and left half. The importance of this symmetrical struc¬ ture lies in the fact that the morphological plane of sym¬ metry is also the dynamical plane of symmetry of the organism. Symmetrical spots of the surface of an animal are chemically identical, having the same chemical con¬ stitution and also the same quantity of reacting masses. Thus the two eyes are symmetrical organs, each contain¬ ing the same photochemical substances in equal quantity. In the eye itself each element is to be considered as chemically identical with the symmetrical point in the other eye. Hence, if the two eyes are illuminated equally,

the photochemical reaction products produced in the same time will be equal in both eyes. What is true for the eyes is true for all symmetrical elements of the surface of an animal. The median plane is also the plane of symmetry for the muscles and the muscular activity of the body. Sym¬ metrical muscles possess under equal conditions equal tension and symmetrical muscles are antagonistic to each other in regard to moving the body to the right or left.

We say that impulses go from the central nervous system to the muscles; and from the surface of the body to the central nervous system. According to our present knowledge that which is called a nervous impulse seems to consist of a wave of chemical reaction traveling along a nerve fiber. The central nervous system is also sym¬ metrical and, moreover, we may conceive a projection of the elements of the surface of the body upon the ganglion cells and from here to the muscular system of the body. The complications in this system of projections consti¬ tute the difficulties in our understanding of the structure of the brain. This idea of a projection of the sense organs or the surface of the body upon the brain will explain why the morphological plane of symmetry of an organism is also its plane of symmetry in a dynamical sense. When symmetrical elements of the eyes are struck by light of the same wave length and intensity, the velocity of photo¬ chemical reactions will be the same in both eyes. Sym¬ metrical spots of the retina are connected with symmetri¬ cal elements in the brain and these in turn are connected with symmetrical muscles. Asa consequence of the equal photochemical reactions in the symmetrical spots of the retina equal changes are produced in the symmetrical brain cells with which they are connected, and equal

chianges in tension will be produced in tbe symmetrical muscles on both sides of tbe body with which the active brain elements are connected.^ On account of the sym¬ metrical character of all the changes no deviation from the original direction of motion will occur. If, however, one eye is illuminated more than the other eye, the influ¬ ence upon the tension of symmetrical muscles will no longer be the same and the animal will be forced to deviate from the original direction of motion.

"We have thus far considered only the relation between right and left. Aside from this symmetry relation we have polarity relations, between apex or head and base or tail end. Just as we found that the morphological plane of symmetry is also a dynamical plane of symmetry, we find that with the morphological polarity head-tail is connected a dynamic polarity of motion, namely, forward and backward. This will become clear in the next chapter on forced movements.

Physiologists have long been in the habit of studying not the reactions of the whole organism but the reactions of isolated segments (the so-called reflexes). While it may seem justifiable to construct the reactions of the a Physiologists assume that stimtilatians are constantly sent from the brain to the, muscles and that this maintains their tension, v. Uexktill uses the term that '*to«nus is sent out to the muscle and that the brain is a reservoir of tonus ” as if the latter were a liquid. The writer wonders whether it might not be wiser to substitute for such metaphors hypotheses in terms of chemical mass action. Constant illumination causes a sta¬ tionary process in photosensitive elements of our eye, in which the mass of the reaction product ie determined by the Bunsen-Roscoe law. We assume, moreover, that in proportion to this photochemical mass action correspond¬ ing chemical reactions take place in the brain elements with which the eyes are connected; and that as a consequence corresponding chemical reactions take place in the muscles by which the tension of the latter is determined. These processes in the muscles may possibly consist in the establishment of a definite hydrog^ ion concentration. Such hypotheses! have the advantage over the ‘^stimulation” hypothesis that they can he tested by physico¬ chemical measurements.

organism as a whole from the individual reflexes, such an attempt is in reality doomed to failure, since reactions produced in an isolated element cannot be counted upon to occur when the same element is part of the whole, on account of the mutual inhibitions which the different parts of the organism produce upon each other when in organic connection^; and it is, therefore, impossible to express the conduct of a whole animal as the. algebraic sum of the reflexes of its isolated segments. '

E. P. Lyon®^® has shown that if the tail in a normal shark be bent to one side (without changing the position of the head) the eyes of the animal move as promptly as compass needles in association with the bent tail around the same axis in which the bending occurs, but in an opposite sense. On the convex side of the animal, the white of the eye is more visible in front, on the concave side it is more visible behind; hence the former has moved backward, the latter forward. This was observed not only in the normal fish but also when the optic and audi¬ tory neiwes were out. The central nervous system acts as one unit. B. Magnus and his fellow-workers have shown that an alteration in the position of the head of a dog inevitably alters the tone of the muscles of the legs.° These and other associations and mutual inhibitions make possible that simplification which allows us to treat the

i>Wli-en the stem of a plant Bryophyllum) is cut into as many pieces as there are nod(^, each node will under the proper conditions give rise to one or two shoots. If we leave them in connection, only the buds at the apical end will grow out, the rest of the buds renaming dormant. The whole stem acts as though it consisted of only the bud situated at the apex. e The problem of coordination will form the subject of another volume in this series by Professor A. R. Moore, and for this reason a fuller discussion of work on coordination, such as that by Sherrington and by v. Uexkttll, may be reserved for Professor Moore^s volume.

organism as a whole as a mere symmetry machine, a simplification which forms the foundation of the tropism theory of animal conduct. It would, therefore, he a misconception to speak of tropisms as of reflexes, since tropisms are reactions of the organism as a whole, while reflexes are reactions of isolated segments. Reflexes and tropisms agree, how¬ ever, in one respect, inasmuch as both are obviously of a purely physico-chemical character. When we destro7 or injure the brain on one side wo paralyze or weaken the muscles connected with this side. As a consequence the morphological plane of symmetry ceases to be the dynamical plane of symmetry and the animal has a tendency to move in circles instead of in a straight line. Suppose a fish swimming forward by motions of its tail fin. Normally the stroke occurs with equal energy to the right and to the left, and the rudder action of the tail is equal in both directions, but after the lesion of one side of the brain the stroke and the rudder action cease to be the same in both directions, it is weakened in one direction. Hence the animal instead of swimming in a straight line is forced to deviate contin¬ ually toward one side from the straight line of locomo¬ tion. We speak in such a case of a forced motion.

When we destroy the ventral portion of the left optic lobe in a shark (ScylUum canicula), the fish no longer swims in straight lines but in circles to the right (when the right optic lobe is destroyed it swims in circles to the left). After the destruction of the left optic lobe, the muscles on the left side of the tail are weakened or semi- paralyzed, and they no longer produce the same rudder action as the muscles on the right side. Hence the im¬ pulses (or nerve processes) which flow in equal intensity to the muscles on both sides will no longer produce equally energetic rudder action of the tail to the right and to the left, but the muscles turning the tail to the right will

contract more powerfully than those turning it in the opposite direction. The outcome of this greater rudder action of the tail when moving to the right is that the fish instead of swimming in a straight line moves in a circle to the right.^*** It is often the case that the body of such a fish even when quiet is no longer straight but bent in a circle, the left side forming the convex side; and when such a fish dies and rigor mortis sets in it may become stiff in this position. These latter observations prove that the circus movements to the right are due to the lowering of the tension of the lateral muscles of the body on the left side of the fish. This is the fimdamental fact for the theory of forced movements—^namely, that a lesion in one side of the brain lessens the tension of the muscles on one side of the body; as a consequence the motions of the animal become difficult or impossible in one direction and become easy in the opposite direction.

In many cases the motions of an animal depend upon a cooperative activity of two sets of appendages, e.g., the pectoral fims of a fish or the legs of an animal. Such cooperative or associated action is determined by the fact that the same nerve center supplies antagonistic muscles of the two organs {e.g., the lateral fins). Thus the same nerve impulse causes both our eyes to move simultaneously to the right or to the left. When we look to the right, the same impulse which causes the contrac¬ tion of the rectus extemus muscle in the ri^t eye causes a contraction of the rectus intemus muscle in the left eye. These two muscles then are associated.'