The Nervous Mechanism of Plants

Another photograph is reproduced (fig. 75, c) of the heliotropic curvature and adjustment of a different species of Sunflower, which was grown in the open. In the morning the plant bent over to the east and all the leaves exhibited appropriate dia-heliotropic movements and torsions. In the afternoon the plant bent over to the west, all the previous adjustments and torsions being completely reversed. The plant continued to exhibit these alternate swings day after day till the movement ceased with age.

It has already been explained that on account of the differential excitability of the upper and lower halves of the pulvinus, a diffuse stimulus causes a responsive fall of the leaf of Mimosa. I shall now show that a similar reaction is manifested by Helianthus. Experiment 80. — In Helianthus, the entire petiole acts as a motile organ, of which the upper half is relatively the less excitable. Diffuse stimulation by electric shock induces a responsive fall, followed by a recovery on the cessation of stimulation. The response-records thus obtained are very similar to those obtained with the leaf of Mimosa. In Helianthus the reaction is relatively sluggish and the contraction is not so great as in Mimosa. The difference between the two responsive reactions is, however, merely one of degree and not of kind.

Response to Stimulation of Upper and Lower Halves of the Organ The pulvinus of Mimosa responds to the application of light from above by contraction of its upper or ventral and expansion of the lower or dorsal half ; the leaf is thus erected, and the movement towards the light may be described as positive heliotropism. The leaflets attached to the subpetioles are thus made to face the hght. Under strong and long-continued sunlight the excitation is transmitted across the pulvinus, causing at first a neutralisation, and finally a reversed or negative movement due to the contraction of the more excitable lower half of the organ. This is the reason why the dia-heliotropic adjustment is less perfect under strong sunlight than under diffuse light.

Experiment 8x.— A parallel reaction is obtained with Hehanthus ; here the petiole acts as an extended pulvinoid. Light applied from above causes an erectile movement; when applied below it causes a more energetic down-movement. As the transverse conductivity of the petiole is feeble, the positive heliotropic response, induced by light acting from above, is rarely reversed into negative. A few words may now be said on the mechanics of the curvature by which the stem of Helianthus bends towards light. All forms of stimulation, including that of light, induce a diminution of turgor and consequent contraction, and retardation of the rate of growth of the directly excited

side. But this is not the only factor in bringing about the positive curvature. I have shown that while the effect of direct stimulation of the proximal side of the stem is to induce a diminution of turgor and contraction, its effect on the distal side, where it acts indirectly, is the very opposite, namely, an increase of turgor and expansion. The positive curvature is thus due to the joint effect of direct stimulation of the one side and indirect stimulation of the other. I have already demonstrated the induced increase of turgor at the distal side in an experiment with the stem of Mimosa (p. 88). The stimulus of light was applied at a point directly opposite to the motile leaf, which by its movement indicates the change of turgor, the induced increase of turgor being indicated by an erection, and diminution of turgor by a fall of the leaf. Application of light at a point on one side of the stem Was thus found to induce an increase of turgor at its diametrically opposite point, as evidenced by the erectile movement of the leaf. (See fig. 33.)

The nervous system of plants must be regarded as of a comparatively simple type. In connexion with the evolution of the animal nervous system, it has been suggested that the contractile tissue or muscle appeared first as an independent effector, and that the nerve developed secondarily in conjunction with the muscles as a means of quickly setting them in action ; that a receptor or sense-organ alone would be of no service to an organism, neither would nerve or nerve-centres alone ; whereas a muscle-cell or effector is of use if it can be stimulated directly.

In plants there are clear indications of these different stages. Thus in the leaf of Erythrina indica, and in the terminal leaflet of Desmodium gyrans, the pulvinus is the independent effector : heliotropic movement only takes place when the pulvinus is direct^ stimulated, illumination of the lamina having no effect ; the connecting nervelink is absent or functionally ineffective. In Mimosa and in Helianthus, on the other hand, the intermediate nervenetwork is effective, the leaflets or the lamina serving as receptive organs. Haberlandt has shown that in many cases the epidermal cells of leaves are of a lenticular shape, for increasing the perception of light. He rightly observes that ‘ in zoological nomenclature, organs concerned with the perception of external stimuli have always been known as sense-organs, even among lower animals and in other cases in which it is doubtful if the organs in question are responsible for sensation in the psychological sense. It is, therefore, not only permissible, but necessary in the interest of consistency to apply the term sense-organ to the analogous structure in plants.’ ^

Since the nervous reactions in animals and plants are so essentially similar, delay in full recognition of this fact will undoubtedly retard the advance of science. I shall in the present chapter demonstrate certain striking effects in plants, which at first sight may no doubt appear to be very surprising, but which can be simply explained as the result of nervous reactions usually regarded as the special characteristic of the animal. I will produce evidence that in the plant a definite nervous link exists between the receptor and the effector, and that there is a weU-developed system of innervation, by which the ‘ attitude ’ of the plant-organ becomes adjusted to the incident stimulus.

I have explained in the previous chapter that the pulvinus of Mimosa is a highly complex organ, its four different quadrants functioning as so many different effectors. When the upper quadrant is directly stimulated by light, there is a responsive up-movement of the leaf ; when the lower quadrant is stimulated, the response is a down-movement. Stimulation of the left quadrant induces ^ Haberlandt, G, — Physiological Plant Anatomy — English translation, I9r4, p. 572.

a left-handed torsion ; that of the right quadrant, a righthanded torsion. The characteristic reaction of each of the quadrants to direct stimulation can also be obtained by the indirect stimulation of the corresponding sub-petiole : this is evidence that a definite nerve-connection exists between each of the sub-petioles and the corresponding quadrant of the pulvinus. The characteristic responses are the same whatever the mode of stimulation, whether mechanical, electric, or photic. Care has, however, to be taken that the stimulus is not too strong, for the effect of excessive stimulation becomes diffused and thus causes a fall of the leaf by the predominant contraction of the lower half of the pulvinus. Electric stimulation by tetanising electric shocks has the advantage that the intensity may be reduced to any extent desirable. Photic stimulation may be effected by throwing light from an arc-lamp on a particular sub-petiole, the intensity of stimulation being suitably increased by prolonging the exposure. The stimulation effected by light is less intense than that caused by electric shocks, and the reaction under light is, therefore, relatively sluggish. The several sub-petioles will be distinguished by definite numbers, counting from the left, the observer being supposed to face the central stem. The sub-petioles (i) and (4) are the two extremes, the two intermediate ones being (2) and (3).

Characteristic Leaf-Movements on Stimulation OF THE Several Sub-Petioles Experiment 82. Response to electric stimulation of s^ibpetioles (i) and (4). — Sub-petiole number (i) was first stimulated by a moderately feeble electric stimulus of short duration ; the response was a left-handed torsion of the leaf, represented by an up-curve. The response was initiated in a short time, and there was recovery on the cessation of stimulation. Sub-petiole number (4) was next

Fig, 76. Record of responses of leaf to stimulation of the several E, torsional responses under electric stimulus ; stimulation of subpetiole I causes left-handed torsion (up-curve) ; that of 4, a right-handed torsion (down-curve), l, similar torsional responses under stimulus of light. The records to the extreme right show the rectilinear responses induced by stimulation of 2 (rapid down-movement) and of 3 (slow up-movement), stimulation induce an identical effect, the sub-petiole (i) was stimulated by throwing on it a strong beam of light from an electric lantern. The response was, as in the last case, a left-handed torsion : stimulation of number (4) induced a right-handed torsion (fig. 76, l).

Experiment 84. Stimulation of sub-petioles {2) and (3).— The responsive movements of the leaf caused by stimulation by light of the two intermediate sub-petioles numbers (2) and (3) were as follows. Stimulation of subpetiole number (2) caused a rapid responsive fall, followed by subsequent recovery on the cessation of light. Stimulation of sub-petiole (3) gave rise to a relatively slow up-movement ; the duration of the exposure to light had, in this case, to be prolonged in order to obtain a moderate amplitude of response.

The effects of direct and indirect stimulation may be summarised as follows : (1) Direct stimulation of the left quadrant or effector (i) induces an anti-clockwise torsion ; indirect stimulation transmitted from sub-petiole (i) produces the same effect. (2) Direct stimulation of the lower effector (2) induces a rectilinear down-movement ; the same effect is produced by indirect stimulation transmitted from sub-petiole (2). (3) Direct stimulation of the upper effector (3) induces a rectilinear up-movement ; the same effect is produced by indirect stimulation transmitted from sub-petiole (3).

(4) Direct stimulation of the right effector (4) induces a clockwise torsion; the same effect is produced by indirect stimulation transmitted from sub-petiole (4). These results prove that there is a definite nervous connection between each sub-petiole and its corresponding quadrant or effector in the pulvinus, such that peripheral stimulation causes the response characteristic of each particular quadrant when directly stimulated (fig. 77). The nerveconnection between the periphery and centre is also independently demonstrated by experiments described in the next chapter (c/. Experiment 85).

Adjustment of Leaf in Space by Transmitted Nervous Excitation Having established the characteristic innervation of the pnlvinus, it is now possible to offer a satisfactory explanation of the dia-heliotropic attitude of the leaf under peripheral stimulation of the sub-petioles by light. When the leaflets, say, of the right sub-petiole, are acted on by vertical light, the distant pulvinus responds Fig. 77. Showing the course of four nerve-strands from the four sub-petioles to the pulvinus. [Mimosa pudica.)

The lower figure is a diagrammatic section of the pulvinus with its four effectors. Effectors i and 4, which give rise to left- and right-handed torsions, are respectively in nervous connection with sub-petioles I and 4. The lower effector 2 is connected with sub-petiole 2, the response being a rapid down-movement. The upper quadrant 3 is in connection with sub-petiole 3, the response being a slow up-moveraent. with a right-handed torsion. The leaflets on the subpetiole are thus carried passively like so many flags, the amount of light absorbed by them being considerably reduced. It is therefore not the advantage of the plant, but the inevitable physiological reaction, that determines the movement. But when the two sub-petioles (i) and (4) are simultaneously exposed to light of the same intensity, the two resultant torsions balance each other. While in this dynamic balance, if the intensity of light on, say, the left sub-petiole (i), be diminished by interposition of a

piece of paper, the balance rs at once upset, and there is a resultant right-handed torsion. Hence the lateral adjustments of the leaf as a whole are made by the two subpetioles (i) and (4) which are situated externally. The balancing adjustments, up or down, are made in response to excitation transmitted by the two middle subpetioles. It is clear that equilibrium is only possible when the entire leaf-surface (consisting of the leaflets carried by the four sub-petioles) is equally illuminated ; and this can only occur when the leaf-surface as a whole is perpendicular to the incident light. The leaf is adjusted in space by the co-ordinated action of four reflexes. The dia-heliotropic attitude of leaves is thus the resultant effect of distinct nervous impulses initiated at the perceptive region and actuating the different effectors at a distance.^

It has been shown that in certain leaves the heliotropic adjustment is brought about by the transmission of nervous impulses from the perceptive to the motor organ. Continuity is shown to exist between the response of ' sensitive ' and that of ordinary plants, Mimosa pudica being the type of the former, and Helianthus annuus of the latter. Mechanical response is brought about in both by the differential excitability of the upper and the lower halves of the motile organ. The lower half in both is the more excitable. Local stimulation of the upper half of the organ induces an erectile movement : that of the lower half, a more rapid downward movement.

Heliotropic curvature of the stem is due to the joint effects of contractile reaction of the proximal and of expansive reaction of the distal side. The pulvinus of Mimosa pudica may be regarded as consisting of four effectors ; under direct stimulation the ^ P'or a more detailed account cf. * The Dia-Heliotropic Attitude of Leaves as Determined by Transmitted Nervous Excitation/ Pvoc. Roy. response of the left effector is by an anti-clockwise torsion, and of the right effector by a clockwise torsion. The upper and lower effectors respond by rectilinear np-and-down movements.

The characteristic responses described above are also given under indirect stimulation. The four quadrants respond to excitation transmitted from the four corresponding sub-petioles when stimulated, the resulting response being determined by the characteristic reaction of the particular effector. Stimulation of the leaflets of sub-petiole (i) by light gives rise to an excitatory impulse which, on reaching the left effector, induces a left-handed torsion ; stimulation of those of sub-petiole (4) induces the opposite or righthanded torsion. Illumination of the leaflets of subpetiole (2) induces a down-movement, illumination of those of sub-petiole (3) an up-movement. The leaf is thus adjusted in space by the co-ordinated action of four reflexes, equilibrium being attained when the leaf-surface is perpendicular to the incident light.

The dia-heliotropic attitude of the leaf, as exemplified by Mimosa pudica, is hioxx^t about by the characteristic reactions of the several effectors in response to transmitted nervous impulses initiated at the perceptive region of the lamina. The definite innervation of the four quadrants of the pulvinus of Mimosa pudica was demonstrated in the last chapter. It was shown that the nerve from the subpetiole (i) is led to the left quadrant ; the sub-petiole (2) is in nervous connection with the lower quadrant ; the central nerve-termination of sub-petiole (3) is in the upper quadrant ; and finally the nerve of sub-petiole (4) terminates in the right quadrant.

I have succeeded in further demonstrating by an independent method the nerve-connection between each quadrant and the corresponding sub-petiole. It consists in observing the effect of stimulating each of the four nerve-ends imbedded in the four quadrants of the pulvinus. In Experiment 19, it was shown that superficial 'scratchstimulus ’ apphed to the sensitive cortex caused contraction and fall of the leaf without exciting the enclosed nerveends. These can be separately stimulated by thrusting a sharp-pointed pin into each of the four quadrants till the nerve-end is reached. After a little practice, it is easy to feel the moment when the pin touches the vascular bundle containing the nerve. It has been explained that the vascular bundles at the centre coalesce into a continuous ring in which the nerves nevertheless remain functionally distinct.

Experiment 85. — When the nerve-end in the left quadrant (i) is cautiously stimulated, an excitatory impulse is generated which travelling outwards causes closure only of the leaflets on sub-petiole (i). Stimulation of the nerve in the lower quadrant (2) causes the same response in sub-petiole (2). Similarly stimulation of the nerveends in quadrants (3) and (4) elicits corresponding response in sub-petioles (3) and (4) respectively. In the following table is given a synopsis of forty different experiments, ten experiments on the stimulation of each nerve-ending. The transmission-time was found by measuring the interval between the application of stimulus and the closure of the innermost pair of leaflets on each sub-petiole. The distance traversed was the length of the petiole plus a very short length of the sub-petiole. The length of the petiole was not exactly the same in the different cases ; the transmission-time is the average of ten different experiments.

Table VIII. — Transmission -time of Impulse from Centre TO Periphery The average transmission-time given in the above table is 24 seconds. In a second series of experiments the average value was found to be 22 seconds. The average transmission-time of the centrifugal impulse from the centre to the first pair of leaflets in the sub-petiole is therefore about 23 seconds more or less. Conversely it is possible to determine the transmissiontime of the centripetal impulse in the petiole initiated by peripheral stimulation. A moderately strong electric stimulus is applied at the middle of one or other of the sub-

petioles. The excitatory impulse travels towards the centre. On account of the intensity of the transmitted excitation, it does not remain localised at one or other of the quadrants, but becomes diffused, causing the fall of the leaf. The transmission-time is measured by noting the interval between the closure of the innermost pair of leaflets on the stimulated sub-petiole and the subsequent fall of the leaf. A detailed account of the results is given in Table IX (p. 182) ; the average value of the centripetal transmissiontime through the petiole, plus the short length of the subpetiole, is 21 seconds. Taking into account the different mode of stimulation and the different batches of plants, the agreement between the transmission-time of this and that of the last series of experiments is remarkably close.

It has been shown that a minimal stimulus applied to one of the four sub-petioles gives rise to an ‘ ingoing ’ impulse which evokes the response characteristic of the corresponding quadrant of the pulvinus. The impulse does not irradiate any further but remains localised. When the intensity of the stimulus is increased, a new and significant class of phenomena makes its appearance, now to be described. Fundamental experiment 86. — A short length of the middle of sub-petiole (i) was stimulated for one second by a tetanising induction-current of moderate intensity. The excitatory impulse, travelling through the length of the petiole in an ingoing or centripetal direction, reached the pulvinus, and caused the fall of the leaf. A rod padded with soft cotton-wool had been placed 5 mm. below the petiole to break the fall. After the arrival of the ingoing or afferent impulse at the pulvinus, it became reflected as an outgoing or efferent impulse, reaching the sub-petiole (2) with resulting serial fall of its leaflets. It has been shown

that an ingoing impulse caused by stimulation of subpetiole (i) reaches the central end in the pulvinus along nerve (i). It has been shown further (Experiment 85) that stimulation of the central end of nerve (2) gives rise to an outgoing impulse which causes response in subpetiole (2), In the present case the central end of nerve (2) was not directly stimulated ; it could only have been excited indirectly by the impulse which reached the central end of nerve (i) as the result of the peripheral stimulation of sub-petiole (i). The afferent impulse must then have overflowed or irradiated from the central end of nerve (i) to that of (2), thus forming an arc ; the reflected impulse now travelled along a new path in an outgoing direction. This is the Reflex arc in Mimosa. The ingoing impulse from the peripheral receptor may be variously described as centripetal, afferent or ‘ sensory ’ : the reflected outgoing impulse may be designated as centrifugal, efferent or ‘ motor.’ The significance of the words in italics wiU shortly become apparent.

In the experiment described, the transmission-time of the afferent impulse from the innermost pair of leaflets of sub-petiole (i) to the pulvinus was 18 seconds, while the transmission-time of the efferent impulse through practically the same distance was only 3 seconds. The velocity of the efferent was found in all cases to he greater than that of the afferent impulse. The relatively high velocity of conduction in the efferent direction is the more remarkable when the total distance which the afferent and efferent impulses had to travel is taken into account : it would naturally be imagined that an impulse would be increasingly impeded the greater the distance it had to travel. But while the primary afferent impulse travelled somewhat slowly in the ingoing direction, after reflection into a new path its velocity was enhanced at least six times.

The essential similarity of nervous impulse in plants and animals has already been demonstrated by the foregoing experiments. The study of the reflex arc in Mimosa is therefore of interest as throwing light on the corresponding phenomenon in the animal. Mimosa indeed offers certain unique advantages. For the moment of arrival of the afferent or ‘ sensory ’ impulse is easily detected by the mechanical response of the main pulvinus at the central end, which serves for the determination of the velocity of the afferent impulse. The interval between the fall of the leaf and the closure of the innermost pair of leaflets of subpetiole (2) gives data for estimating the velocity of the efferent impulse. Again, as the velocity of the nervous impulse in Mimosa is about 1000 times slower than that in the animal, any difference in the velocity of afferent and efferent impulses is easily detected in the plant; this is practically impossible in the animal.