Technique. Observations were made on 25 skates caught by trawl. by a small transverse wound in the mid-dorsal line immediately behind
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1 THE SPINAL REFLEXES OF THE SKATE. BY C. HELEN CRAW (Richardson Fellow in Anatomy, University of Toronto). (From the Atlantic Biological Station, St Andrews, New Brunswick.) THE skate is an Elasmobranch, belonging to the genus Raja. It is a relatively hardy animal and suitable for experimental studies. The "spinal" skate is easily prepared and can be kept alive for weeks. Its reflexes are numerous and lend themselves yvell to observation. Technique. Observations were made on 25 skates caught by trawl and removed to the laboratory tanks which contained running sea water. The skates were largely Raja erinacea Mitchill and averaged 20 inches in length. They remained in the tanks two days, at the end of which time they appeared normally active. Without removing the skate from the water, we cut between the medulla oblongata and the cord, entering by a small transverse wound in the mid-dorsal line immediately behind the most posterior part of the skull. Heemorrhage was controlled by plugging the wound with cotton. In 50 p.c. of the cases, the respiratory movements continued normally. In the other 50 p.c. they ceased or appeared weak and irregular. In the latter cases, we inserted a tube of running water into the mouth and allowed the stream to run out over the gills. Normal respiratory movements having returned within an hour we removed the tube. In a few cases we destroyed the brain; respiratory movements never then returned, the tube method of artificial respiration being used the whole time Ȯbservations were made with electrical, thermal and chemical stimiuli; but the mechanical proved so satisfactory and convenient that it was adopted entirely. Both ventral and dorsal surfaces of the skate were investigated by pinching with metal forceps, and by light touch and stroking with the same instrument. These experiments are summarized in Table I, which should be read in conjunction with Figs. 1 and 2. The response to stimulation of the posterior pectoral border (Area E, Fig. 1) is bilateral, usually a little weaker on the contralateral side.
2 62 C. H. CRAW. TABLE I. Reflexes of the Spinal Skate in Response to Mechanical Stimuli. Receptive area Stimulus Response Ventral surface (1) Abdominal region (A) Stroking or pinching the skin A general ventral contraction of all the fins and of the tail (2) At base of pelvic fin (B), Light touch A ventral flexion of the distal area stretches out along part of the anterior lobe of the the fin pelvic fin (unilateral) (3) Pectoral fin-mid-ventral surface (C) Stroking Curling of ventrally the edge of the fin (4) Tail-ventral surface Stroking and Strong posterior rotation (adpinching duction) of the pelvic fins so that their posterior lobes overlap across the mid-line in front of the tail (5) Lateral border of pec- Pinching edge Curling of edge of fin ventrally. toral fin-anterior a When stimulus is repeated the (D) curling is followed by avigorous dorsal flip of the whole fin (6) Lateral border of pec- Pinching edge Ventral curling of pectoral fintoral fin-posterior half anterior rotation (abduction) of (X) anterior lobe of pelvic fin-a lateral movement of tail to side of stimulation (7) Pelvic fin-tip of an- Pinching Ventral flexion of distal part of teriorlobe andposterior anterior lobe. When stimulus border of anterior lobe is strong-there is also a ven- (F) tral curling of the pectoral fin (8) Lateral border of pos- Pinching Rotation of pelvic lobe-generterior lobe of pelvic fin ally in a posterior direction but (G) sometimes the posterior rotation is followed by anterior rotation which position is maintained Doral surface (9) Midline-particularly in Stroking heavy Dorsal arching of the tail and region of pelvicgirdle(j) raising of the anterior part of the body, so that the pelvic region and the tip of tail only touch bottom of tank (10) Soft part at the base of the pectoral fin (K) Light touch A dorsal curl of the pectoral fin (11) Ditto (K) Stroking A ventral curling contraction (12) Tail Pinching whole thickness of tail Lateral movement of body and tail to same side (13) Dorsal fins and tip of tail Pinching Lateral movement of body and tail which, if the stimulation is continued alternates from side to side and is accompanied by rotatory movements of the pelvic fins. The whole reflex if strong causes the skate to swim forwards
3 THE SPINAL REFLEXES OF THE SKATE. 63 The lateral border of the pectoral fin curls strongly in the ventral direction, the anterior lobe of the pelvic fin rotates in the anterior direction (abducts) and -ften flexes ventrally. The tail moves to the ( t - i ~~~~~~~~Abdominal - Pectoral fin Anterior lobe of pelvic fin P lsteroriobe of pelvic fin Fig. 1. Areas of receptivity on ventral surface. ipsilateral side. A pinch of the edge was the commonest stimulus used, but when the skate is very reactive a light tap suffices. The reflex afterdischarge is sometimes very long (1-5 minutes). It can be inhibited by the posterior rotatory reflex arising from stimulation of the tail. It is among the first to appear and the last to disappear. The response appears first in the pectoral fin, then in the pelvic fin, and later in the tail, and disappears in the same order. When the response of the tail is very strong the contralateral pelvic lobe is often drawn down in a posterior direction. When the skate is lying on its ventral surface the response of the contralateral fin is often an undulating wave of contraction, similar to that seen in the pectoral fins when the skate is swimming. The dorsal surface is much less sensitive than the ventral. Comparison of the two responses from area K (Fig. 2) is interesting. The response to light touch can only be elicited after a number of stimuli
4 64 C. H. CRAW. (8-12) are given. If stimulation is discontinued the pectoral fin arises only a few centimetres and then falls, but if it is continued the whole Fig. 2. Dorsal surface. fin will make a complete curl so that the lateral edge touches the middorsal region. The response to stroking in the same area is by ventral curling which tucks the peripheral part of the fin under the rest of it. In two skates the stroking had to be very severe or the response was similar to that from touch stimulation. I detected no period following the spinal operation in which all reflexes caudal to the section were absent. The reflexes were usually weak, increasing in strength gradually for the first hour. Extreme reactivity was observed 1 to 3 hours after operation; a very light touch then elicited a response. This extreme sensitivity gradually disappeared and the skate then showed the regular responses as listed above. Immediately after operation, if the skate were held up by its tail, the pectoral fins fell down in a limp manner so that their borders almost met in the mid-ventral line. The normal skate so held flaps these fins,
5 THE SPINAL REFLEXES OF THE SKATE. or if quiescent they hang in a more lateral posture with the peripheral part lifted dorsally. In the second week after operation, the fins gradually recover this posture. With care the spinal skate would live for months. I took no aseptic precautions in my operations. The skate is extremely sensitive to anoxaemia. One spinal skate lying in a small tank of still water exhibited very weak responses in three-quarters of an hour and total absence of them in two hours. When the taps were turned on again the reflexes recovered and lasted some days. 0 One skate showed active responses at the end of six weeks. I fed the skates with a little fish muscle, putting the food into the back of the mouth. Digestive operations appeared normal. Normal egg-cases were laid by three of the spinal skates. Life habits. I studied the swimming and feeding habits of the skate for possible relations of the reflexes to these activities of the normal animal. The skate, unlike the shark and other members of the Raja group, is a sluggish animal living on the bottom of the sea. Its mouth is on the ventral side of its head. It obtains its food (molluscs, crustaceans and smaller fish) by approaching them quietly, and swimming right over them. It pins its prey down between its own body and the sea-bottom, and by quick movements of the fish fins, the prey is carried by water currents to the mouth and devoured. I have observed that when one attempts to lift the skate up by the tail, it often resists with a strong hold of the fins on the bottom of the tank. Sometimes in drawing up the trawl, a very severe tug is necessary to bring the skate from the bottom, showing that the flexor muscles must be very strong. There seem to be two types of locomotion. In one the anterior lobes of the pelvic fin are used against the bottom of the tank, usually together but sometimes separately, while the pectorals exhibit undulating moyements. In the second and more rapid type of swimming the whole fish is off the bottom of the tank. The anterior lobes of the pelvic fins are held far posteriorly, and the locomotion is-carried out by the rhythmic undulations of the pectorals. The tail is used as a rudder, but in rapid swimming it may be "swished" from side to side. In turning, the head end of the animal and the tail approach towards the side of turning-the pelvic fins being usually used against the bottom. Investigating one Raja radiata, I found strong reflexes which varied in certain ways from the responses of Raja erinacea. For example, the pectoral edge reflex' elicited a posterior rather than an anterior PH. LXULI 5 65
6 66 C. H. CRAW. response in the pelvic fins, which were shorter and thicker than in Erinacea. Anatomical notes. The pectoral fin border can be divided by its innervation into two parts which correspond roughly with receptive areas D and E (Fig. 1). The anterior part is supplied by the most anterior pectoral fin nerves, which, after passing out of the vertebral canal, form a "brachial" plexus. The posterior half is supplied by nerves which remain distinct throughout their course and innervate successive small areas of the fin. They run in a postero-lateral direction across the soft part of the back (the region between the girdles) lying just external to the peritoneum. Reaching the metapterygium of the pectoral fin they divide. A small branch runs around to supply the ventral musculature while the two terminal branches run still postero-laterally on either side of the metapterygium, one supplying the dorsal and the other the ventral muscle layers. The pelvic fin is supplied by twelve nerves, six going to the anterior and six to the posterior lobe. The first nerves form a plexus of a simple kind. Distal electrical stimulation of the cut end of a pectoral fin nerve caused a movement of the corresponding part of the fin covering about three to five fin rays. Distal stimulation of the first two pelvic nerves caused anterior rotation of the anterior lobe, of the fourth and sixth posterior rotation of the same, while the last six nerves ventral curling of the posterior lobe. By central electrical stimulation of the cut ends of the sixth to the eighth pectoral nerves I obtained anterior rotation of the anterior lobe of the pelvic fin. Results of transection, total and partial, of the cord. The cord was exposed by removing the appropriate lamina from the dorsal aspect. Experiments showed that the extent of exposure of the cord should be as small as possible. As the hsemorrhage is often considerable, bleeding from the muscles of the wound was controlled by cautery. In one very active skate the spinal column was opened to the extent of 3 to 4 inches. The animal lived four days, but never recovered active reflexes. With exposure of the cord just sufficient for operation, the reflexes recover in 10 to 15 minutes. In choosing my level for transection I regularly counted eight vertebrae back from the pectoral girdle and entered posteriorly to the eighth, but there is much variation in the relation of cord to vertebrae. It is possible to isolate between complete transverse sections the part of the cord which contains the centres and receives the nerves of a par-
7 THE SPINAL REFLEXES OP THE SKATE. ticular reflex. I have isolated the cord segments for the pelvic fin between two sections, one anterior to the first nerve to the pelvic fin, and the second twelve nerve segments further back. Immediately after the-final section, all reflex activity is lost, but begins to return in 10 minutes. A pinch of the edge evoked rotation and ventral flexion of the anterior lobe of both ipsilateral and contralateral fins. In addition the back arched and the tail moved slightly. This movement of the tail must be entirely due to the action of the back muscles above the second lesion because pinching the tail caused a lateral movement of the tail, but no response in the pelvic fins. I was able to isolate the posterior pectoral curl in response to pectoral pinch, but never got any satisfactory isolation of the anterior pelvic rotation reflex in response to pectoral pinch. I cut one half of the cord between the most posterior nerves supplying the pectoral fin and the most anterior supplying the pelvic, and used the reflex from the posterior pectoral edge (Area E, Fig. 1) to test the results. In my first experiments I did not allow for a recovery period and judged that all responses of the pelvic fin from stimulation of the pectoral edge of the injured side were eliminated, while those of the uninjured side remained strong ipsilaterally and weak contralaterally. After a short period, however, all reflexes began to return. On the intact side, the ipsilateral response was strong, the contralateral weak, while on the sectioned side the ipsilateral was weak and the contralateral fairly strong. In one skate with very strong reflexes I made a right semisection in the usual place. Ten minutes after the operation both pectoral fins responded to pinching of the edge by a strong ventral curl. The only response of the pelvic fins was the ipsilateral response of the left (uninjured) side. In an hour the responses of the pelvic fins from stimulation of the right side had begun to reappear. The tail responded to stimulation on the left side but showed no response on the right. In four hours the right side showed a strong contralateral pelvic fin response and a response of the tail, which however was always away from the side stimulated. After 24 hours the skate was in good condition. The tail always moved to the left (uninjured) side and the right pelvic fin rotated posteriorly. Thus stimulation of the right (injured) side yielded a strong contralateral anterior rotation, a weak ipsilateral posterior rotation and a very weak movement of the tail to the contralateral side. In response to stimulation of the left (uninjured) side I received a strong ipsilateral 67
8 68 C. H. CRAW. anterior rotation of the pelvic fin, a weaker contralateral posterior rotation, and a remarkably strong lateral movement of the tail to the ipsilateral side. This position of tail strongly curled to the left, right pelvic fin posteriorly rotated and left pelvic fin anteriorly rotated, was often held for a very long time. It is illustrated diagrammatically in Fig. 3. It could sometimes be elicited by abdominal stimulation. Fig. 3. The pelvic fins were very sensitive. Pinching their edge caused a posterior rotation of both pelvic fins, and a lateral movement of the tail to the stimulated side-thus the tail moved to the right side when the right pelvic fin was stimulated but to the left when the right pectoral fin was stimulated. By the fourth day the reflexes were weaker. The extent of spinal crossing of nerve-impulses is evidently considerable. Microscopic examination of the lesion showed that the gray matter of the right side has been destroyed completely and the dorsal, lateral and a large part of the ventral columns of the white matter. The ventro-mesial corner of the ventral column was not cut. The left half of the cord was intact.
9 THE SPINAL REFLEXES OF THE SKATE. 69 SUMMARY. 1. A "spinal" skate is a very suitable preparation for studying of reflexes. 2. Different types of its spinal reflexes are described. 3. Influence of total and partial transection of the spinal cord on the spinal reflexes is described. I wish to thank Professor B. P. Babkin of Dalhousie University for suggesting the problem and for his active cooperation, Professor J. J. R. M a cl e o d of the University of Toronto for advice, and Dr A. G. Hunts man, Director of the St Andrews Biological Station, for arranging for the obtaining of the material required.
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