Proprioception In Insects

467

PROPRIOCEPTION IN INSECTS

III. THE FUNCTION OF THE HAIR SENSILLA AT THE JOINTS

BY J. W. S. PRINGLE, M.A.

From the Zoological Laboratory, Cambridge

(Received 4 March 1938)

(With One Plate and Five Text-figures)

INTRODUCTION

LOWNE (1890) described an organ, which he called the "prosternal organ", from

the extreme anterior part of the thorax of the blowfly. This seems to be the first mention in the literature of the peculiar concentrations of hair sensilla which are to be found near the joint surfaces in many parts of the insect body, and whose function presents an interesting problem.

Lowne's figure of the prosternal organ of CaUiphora is reproduced in Text-fig. 1. It consists, in his words, of "a plate covered with long fine setae, beneath which

Text-fig. 1. The prosternal organ of CaUiphora (from Lowne, 1890). b., basal part of head;

c, neck sclerite; con., connecting membrane; n., nerve; pth., prothorax.

there is a layer of large ganglion cells connected with a branch of the prothoracic dorsal nerve. The setae are on an average o-i mm. in length and each apparently receives a process from one of the subjacent ganglion cells". Of its function he says "the deep-seated position of this organ renders it most improbable that it is a tactile organ. I ventured to suggest that it is concerned in registering as it were the movements of the head and fore limb, but with the further knowledge of its structure which I now possess I entertain the gravest doubts of the possibility of such an explanation of its function."

Periplaneta americcma. He found the change in the position of this joint when the

limbs no longer supported the weight of the body to be an important factor in initiating flight movements.

More direct evidence of the existence of sense organs sensitive to joint move-ment was provided by Barnes (1931) who used the electrical recording technique to study the nerve impulses in the sensory nerves from the leg of Periplaneta. Barnes found there that movement of the joints produced impulses in the leg nerve, and that the adaptation of the sense organs concerned was rapid. He did not describe the endings, but identified them tentatively with the joint hairs.

Pringle (1937) extended this work and found that many of the impulses in the leg nerve during joint movement arose not from the hairs, but from the campani-form sensilla at the joints. During the course of that investigation, however, a number of structures were discovered which appeared to resemble closely the organ described by Lowne from the blowfly, and to suggest a possible function for such organs.

MATERIAL AND METHODS

The American cockroach, Periplaneta americana L., has been used for this work, and the method is also similar to that used in the previous investigations (Pringle,

1937). The nerve from the sense organs is dissected out and placed on fine platinum wire electrodes, which are connected to a four-stage condenser-coupled amplifier feeding a Matthews (1928) oscillograph and loud-speaker.

RESULTS

(1) Isolated hairs

In the joints of nearly all the appendages of Periplaneta and in the interseg-mental membranes of the body, there are to be found small scattered hair sensilla. Not all of these are provided with sensory nerves, but some were found both in the joints of the maxillary palp and on the trochanter, which gave rise to impulses in the nerve when they were moved with a fine needle. In all cases adaptation was rapid, and in many the discharge persisted only for so long as the hair was moving. These hairs can often be seen to be disturbed, during extreme flexion or extension of the joint, by the cuticle of the next segment, and they should therefore serve to register momentarily such movements.

(2) Hair plates

Proprioception in Insects 469

organ of the blowfly. The appearance of the plates in cleared and potashed pre-parations is shown in PI. I, figs. 1, 2. The hairs themselves are less heavily sclero-tized than the plate itself, and their bases appear as clear round holes in the cuticle. The number of hairs on the plates of each leg is given in Table I, compiled from a single average-sized individual.

The two coxal hair plates are innervated from the smaller of the two nerves that supply the leg, the trochanteral hair plate from the large nerve. The experi-ments to be described have been made on the inner coxal plate, which is the most accessible, and whose impulses are most easily recorded owing to the smaller number

o.h.p.

tr.arL

Text-fig. 2. The 2nd leg of Periplaneta. ex., coxa; i.h.p., inner coxal hair plate; o.h.p., outer coxal hair plate; tr., trochantin; trMrt., trochantinal articulation of coxa; tr.h.p., trochanteral hair plate.

Table I. Number of hair sensilla on the hair plates of the legs of Periplaneta

Thoracic segment

I.

I I .

III. C O1UC R. L. R. L. R. L. Av. Av. Av. Outer coxal hair 42 37 1 2 IO 1 2 IO plate 3 9 1 1 1 1 Inner hair 83 79 63 75 75 7 i coxal plate 8 1 69 7 3 Trochanteral hair 43 41 45 46 56 53 plate 4 2 4 5 64

of other fibres in the small nerve trunk. The results have been confirmed on the trochanteral plate.

Stimulation of the hairs of the inner coxal plate with a fine needle point produces impulses in the nerve. Owing to the close packing of the hairs it is impossible to move one hair alone without disturbing the others, and the impulses are usually confused. Occasionally, however, records are obtained which appear from the regular rhythm to show the activity of a single fibre (PL I, fig. 3). The initial fre-quency may be very high (over 800 per sec. has been recorded at 210 C.) and it falls off slowly to a steady level which is maintained for a long time (Text-fig. 3).

diagram-matically how this occurs, for the case of the inner coxal plate. The coxa articulates to the pleuron at two points (Text-fig. 2), and its chief movement is a rotation about the line joining these two. In this rotation the part of the cuticle bearing the inner coxal hair plate slides under the edge of the pleuron and the hairs are brushed down by the intersegmental membrane. PI. I, fig. 2, of the trochanteral hair plate, shows the natural position of the hairs, which have been fixed in the position they take up in life. Though the intersegmental membrane has been removed after fixation, the curve where it touched the hairs is still clearly visible.

8001-5 6 Seconds

10

Text-fig. 3. Graph showing the adaptation of a nerve ending on the inner coxal hair plate of

Periplaneta to the stimulus of a constant deflexion of the hairs. Two records from the same

preparation.

ex.

Text-fig. 4. Diagram to show the method of excitation of the inner coxal hair plate by a fold of the intersegmental membrane, ex., coxa; tup., hair plate, pi., pleuron.

Proprioception in Insects 471

One other noteworthy feature must be mentioned. The hairs of the plates are sensitive to movements of extremely small amplitude, and if a slight vibration be imparted to the stimulating needle, a large synchronized discharge can be detected in the nerve (PL I, fig. 4). In several cases the sound from the loud speaker, several feet away from the preparation, was sufficient to maintain the vibration of the needle, and the synchronized discharge would then continue for several minutes until the needle was moved. At such times the vibration of the needle point was invisible under a magnification of 100 x .

DISCUSSION

Two functions for the hair plates suggest themselves from the above experi-ments. On the one hand one can suppose, with Lowne, that the plates serve to register the position of the joints at which they lie. In favour of this interpretation are the following points:

(1) The sensory discharge from the hairs is incompletely adapting and the frequency, after an initial decline, continues at a constant level almost indefinitely. Such a behaviour is well suited to sense organs registering a static phenomenon such as position.

(2) The activity in the whole nerve trunk will depend on the degree of excitation of the individual hairs and on the total number excited. Both these will increase according to the degree of flexion of the joint, and the total activity in the nerve trunk could give an indication of the joint position. The activity has been shown to increase during depression in the case of the inner coxal plate.

(3) It will be seen from Table I that the only significant difference between the number of hairs on the different legs is the relatively greater importance of the outer coxal hair plate on the first pair. This plate is situated close to the pleuro-coxal condyle, about which there is a considerably greater degree of rotation possible in the first legs than in the other two pairs. The outer coxal hair plate could register the extent of this movement.

(4) The hair plates are situated on the most basal joints of the legs, where the greatest accuracy of movement is necessary owing to the length of leg distal to the joint. It has been found similarly in man (Goldscheider, 1889) that there is a more accurate joint sense at the shoulder than at the elbow or fingers.

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same way as has been described by Magnus (1924) for vertebrates. That such fixation can occur in insects has been shown by Roeder (1936) for the mantis, where the prosternal organ is exceptionally well developed (Text-fig. 5).

We may conclude, then, that Lowne's original conception of the role of these joint hairs is in all probability correct. Experimental work on the responses aroused by their stimulation is obviously necessary to settle their function beyond all doubt;

pr.

Text-fig. 5. The left prosternal organ of a mantis, b., basal part of head; n., neck sclerites;

pr., prosternal organ.

but if they do introduce a "position" sense for certain of the more important move-ments in insects, they will add another part to the proprioceptive system, and may provide more convenient material for studying the workings of a static sense than has so far been found in the Vertebrates.

SUMMARY

1.. Concentrations of hair sensilla have been noted by a number of authors in the joints of the insect body and limbs.

Fig. 1. Fig. 2.

Fig.

3-Fig.

Proprioception in Insects 473

3. The hairs of the hair plates are mechanical sense organs with a slow rate of adaptation.

4. In life the hairs are excited by a fold of the intersegmental membrane, the excitation varying with the position of the joint.

5. It is suggested that these and similar structures in other parts of the bodies of insects act as "position" sense organs.

I am indebted to Mr E. W. Mynott for the illustration in Text-fig. 5.

REFERENCES

BARNES, T. C. (1931). Ann. ent. Soc. Amer. 24, 824. DIAKONOFF, A. (1936). Arch, nierl. Set. 21, 104. GOLDSCHEIDER, A. (1889). Arch. Phytiol. p. 369. LOWNE, B. T. (1890). The Blow-fly. London. MAGNUS, R. (1924). Korperttellttng. Berlin. MATTHEWS, B. H. C. (1928). J. Phytiol. 66, 225. PRINGLE, J. W. S. (1937). J. exp. Biol. 15, 114.

ROEDER, K. D. (1936). Biol. Bull. Wood's Hole, 69, 203.

EXPLANATION OF PLATE I

Fig. 1. Photomicrograph of the inner coxal hair plate of Periplaneta.

Fig. 2. Photomicrograph of the trochanteral hair plate of Periplaneta, showing the natural position of the hairs.

Fig. 3. Oscillograph record of the discharge from a single nerve ending in the inner coxal hair plate to the stimulus of a constant deflection of the hairs.

Fig. 4. Oscillograph record of a synchronized discharge from the inner coxal hair plate to the stimulus of a vibrating needle point.