Orbeli are of sympathetic origin. Moreover he found relatively little
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1 THE SYMPATHETIC INNERVATION OF THE SKIN OF THE TOAD. BY K. UYENO. THE general scheme of sympathetic innervation in the frog has been determined by Langley and Orbeli(i) on the basis of the visceromotor fibres and by Langley(2) on that of the vaso-motor fibres. In the toad it was investigated by Langley and Orbeli(3) by the degeneration method. They concluded that the scheme in broad features was the same as that shown by Langley in the mammal and bird. E. J. BrUcke(4) in recent experiments on the innervation of the skin glands of the toad describes results which do not harmonise with this conclusion. According to him, sympathetic secretory fibres occur in the roots of the spinal nerves giving origin to the pelvic nerve, and in consequence he suggests that the sacral autonomic nerves of Langley and Orbeli are of sympathetic origin. Moreover he found relatively little overlapping in the areas of the skin of the trunk supplied by the successive spinal nerves and a much less extensive origin of the secretory fibres supplying the hind limb than that given by Langley of the vaso-constrictor fibres. In view of these experiments, I have, at Prof. Langley's suggestion, re-investigated the origin of the sympathetic fibres supplying the skin glands of the toad. Method. The toads weighed about 25 to 50 grms.; 0-2 to 0 5 c.c. of 25 p.c. urethane was injected subcutaneously into the dorsal lymph sac. This dose, which was about half that used by Briicke, was given since it was found in general that a larger one decreased the amount of secretion obtained. The cerebral hemispheres and a part of the midbrain were destroyed and the spinal cord exposed. The dura mater was cut through, the 8th to the 10thl posterior roots of both sides and the cauda equina were tied separately and cut peripherally of the ligatures. Lifting the ligatures all the remaining spinal roots, both anterior and posterior, were cut at the nearest point to the cord and the spinal cord was removed. The roots floating in the blood and cerebro-spinal fluid were lifted with a fine hooked probe, placed on the edge of the spinal canal and tied with thin silk. The fine anterior and posterior roots of the 3rd to the 6th nerves were generally tied and stimulated together. I The hypoglossus is here enumerated as the first spinal nerve so that the 8th to the 10th roots in this text correspond to the 9th to the 11th in Briicke's description.
2 360 K. UYENO. The 1st spinal root I found too short and delicate for isolation, but both Langley and Brucke state that the 1st spinal nerve does not send fibres to the sympathetic. Another delicate root, the 10th, was generally stimulated with the 9th and isolated in a few cases only: Experiments were made on twelve toads and as a rule all the spinal roots except the 1st were stimulated. The roots can be distinguished with fair certainty by the muscular contraction they produce on stimulation. The 2nd, which of course can be told by its size, causes extension and adduction of the fore-limb. The 3rd to the 7th cause contraction in successive portions of the abdominal wall; the 3rd produces also slight flexion and pronation of the fore-arm, whilst the 7th causes adduction of the thigh. The 8th causes extension of the leg and flexion of the toes and the 9th extension of the leg and toes. The effect of stimulating the 8th and 9th depends on whether the arrangement of the nerves is anterior or posterior. The facts mentioned above refer to the general case; in the extreme posterior arrangement, weak stimuli applied to the 9th cause flexion of the toes while stronger stimuli cause extension. The heart was not cut out, as it was in Briicke's experiments, since this abolishes the slight circulation that may remain after the operation. The clotting of blood in the spinal canal I found rather advantageous than otherwise, since the white roots floating in the red clot were easily,seen. Results. As in Brnicke's experiments the amount of the secretion obtained on stimulating any given nerve root, and the extent of the area in which secretion occurred, varied considerably in different experiments, and to a degree outside any possible difference of anterior and posterior arrangement of nerves. There is no warrant for thinking that these differences are due to differences of innervation in different toads. They may I think in the main be attributed with certainty to differences in excitability caused by differences in the state of the circulation. It is known that the response given by pre-ganglionic fibres decreases with decrease of blood flow. By my method of operation the blood is slowed to an indeterminate extent, by B ruicke's method the circulation ceases. The secretion obtained by stimulating nerve roots immediately after the operation described above is more copious, and the area affected more extensive than that obtained by stimulating it half-an-hour later and the later stimulation may have no effect. Recovery is slow in amphibia, and it is especially slow in absence of circulation; thus when nerves are stimulated in succession, stimulation of one tends to reduce the response of all others which supply the same glands. How far the glands are innervated by more than one spinal nerve I have not noted, but I have seen the same gland on the leg secrete on stimulating either
3 SYMPATHETIC OF TOAD. the 8th or the 9th nerve. It follows from these considerations that the most extensive area affected in any one experiment most nearly represents the normal innervation in all. In the figures I give the maximal Maximal area of secretion obtained by stimulation of the 2nd to the 8th nerves. The dots represent roughly the amount of secretion. areas in which I have obtained secretion with each spinal nerve, how often they have been obtained I mention in the detailed account. I regard them as showing fairly accurately the normal innervation. Accurate results can probably only be obtained in toads with a normal circulation. I may consider first the points which concern the general arrangement of the pre-ganglionic sympathetic fibres. The most fundamental is the origin of sympathetic fibres from the nerves giving origin to the pelvic nerve (sacral autonomic). According to Langley and Orbeli the pelvic nerve arises from the 9th and 10th nerves and these containing no sympathetic pre-ganglionic fibres, they found (3) that section
4 362 K. UYENO. of the roots of the 9th nerve in the toad caused either no degeneration in the sympathetic or only of one or two fibres, and that it caused degeneration of numerous fibres in the pelvic nerve. I have stimulated the anterior root of the 9th nerve in 20 experiments (preliminary and supplemental experiments included) in which other nerves caused secretion and have never found that it caused secretion. I consider then that Briicke's result must have been due to escape of current to the postganglionic fibres. Briicke mentioned that he found it necessary to use relatively strong currents. A less important point is the degree of overlapping of the pre-ganglionic fibres of different nerves. According to Briicke, the skin of the back receives secretory fibres from at most two nerves, and the highest nerve which sends secretory fibres to the hind limb is the 6th or occasionally the 5th nerve. I find that each area of the skin of the back is innervated by three nerves and there is some evidence that parts are innervated by four nerves. I find also that the skin of the hind limb may receive secretory fibres from the 5th, 4th and 3rd nerves as well as from the 6th, 7th and sometimes from the 8th. There is then no reason for supposing that the origin of the sympathetic fibres in amphibia differs in any essential way from that of the mammal or bird and I pass to the consideration of some details of the distribution of the fibres of each nerve root. 2nd nerve. The 2nd root is so short that it is not easy to tie without tearing it. Hence the electrodes were generally placed on the roots as they lay on the side-wall of the spinal canal. This method makes it difficult to exclude the possibility of escape of current to the 3rd nerve, and the secretory area for the 2nd nerve marked in the figure I give with reserve. In all cases in which the stimulation of the 2nd root was effective, it never failed to produce some secretion in the head. The area of greatest secretion varied, and sometimes it was nearly equal in all parts of the head. Secretion occurred sometimes in the upper region of the back and in one case it was good in nearly the whole of the back. On the fore-limb secretion was obtained four times. 3rd nerve. The 3rd nerve generally produced copious secretion in the head and upper region of the back. Frequently there was secretion in the whole of the back and in all cases but one in the fore-limb. In three cases secretion occurred also in the hind-limb, in one it occurred boti, in the fore and hind limb. In two there was slight secretion in the thigh. In one the secretion was fairly good in the thigh and leg, slight in the foot; this result was obtained with a weak current, one very near the threshold. On the whole the 3rdnerve caused a somewhat greater secretion
5 SYMPATHETIC OF TOAD. 363 on the head than the 2nd nerve; in four out of six experiments the 3rd nerve had a slightly stronger effect than the 2nd; in one it had a markedly greater effect but in one it was distinctly less and confined to the posterior part of the head. The 3rd root was found slightly larger than usual when it produced good secretion in a wide area. In two cases there was a fairly large communicating bundle between the 2nd and 3rd nerves inside the spinal canal on the right side, the left side being normal; an arrangement which has not so far as I know been noted in any animal. 4th nerve. In three experiments the 4th nerve on both sides, and in four experiments the nerve on one side failed to cause secretion. The secretion when obtained was freest on the back though sometimes it was restricted to a part of the back. In two cases a few drops of secretion were observed in the prominence (parotid) behind the eye and in the small area on the side of the head below it. In one case secretion occurred also inr the hind-limb, fairly good in the thigh and leg and slight in the foot. In two cases some secretion was obtained in the fore-limb. As with the 3rd nerve secretion in one experiment was obtained both in the fore and hind limb. In two cases the 4th affected the whole of the back and the 3rd produced good to copious secretion in the upper region of the back but none or slight in the lower part. 5th nerve. The 5th nerve failed to produce secretion in four experiments on both sides and in four experiments on one side. In the other experiment the secretion in the lower half of the back was good, occasionally extending to the upper region. In two cases there was good secretion in the hind-limb and in two a trace. In one case there were a few drops in the small area on the side of the head below the " parotid." The secretion caused by the 4th and 5th nerves was less than that caused by the 2nd, 3rd, 6th or 7th. Probably they contain relatively few secretory fibres, so that with failing circulation they are the first to cease to have an effect. 6th nerve. Secretion occurred in the lower half of the back and near the anus but not in the upper half in nine experiments; in all but one, the nerve produced secretion in the hind-limb. 7th nerve. This had generally a good effect in the lower region of the back and never failed to cause secretion in the hind-limb, it was especially free in the leg. The area innervated by the 7th nerve did not extend quite so high as that of the 6th. The effect in the hind-limb and the region near the anus was always greater with the 7th than with the 6th nerve. 8th nerve. In five toads out of 20, including preliminary and supplementary experiments, this produced some secretion confined to the
6 364 K. UYENO. hind-limb. In no case was the secretion greater than with the 7th; in three cases it was much less, and in two slightly less than with the 7th. In each of the five experiments the area of secretion was nearly the same as with the 7th. Variation in lower spinal nerves. As was pointed out by Langley the variation in the arrangement of the lumbar plexus is not marked in toads. I have paid attention to the size of spinal roots and nerves in several toads especially when the 8th root was effective. In the 7th to the 9th nerves the posterior root is usually larger than the anterior root, the 8th and 9th being nearly of the same size and much the same in different animals though there is slight variation. On the other hand the size of the 8th and the 9th anterior roots varies greatly. In extreme cases either the 8th or the 9th can be twice as large as the other and in such cases it can often be followed in two bundles to the spinal ganglion. Slight variation in the size of the anterior roots does not always reveal itself in the lumbar plexus, sometimes the variation is the reverse of that in the anterior roots. Still there seems to exist some relation between the size of the anterior roots and the presence of the sympathetic fibres in the 8th root. In three out of five toads in which secretory fibres were found in the 8th root, the 9th anterior was twice as large as that of the 8th, in one the 9th nerve was larger than the 8th. Though this suggests the posterior arrangement of the anterior roots in the lumbar plexus, there was still one case in which the 8th anterior root was effective and slightly larger than the 9th anterior root. The 7th anterior root looked rather smaller than usual in these cases but no accurate estimation was made. In four other cases in which the 8th root had no effect the 8th anterior root was either much larger than the 9th and in two bundles, or of nearly the same size. I conclude that variation occurs chiefly in the 8th and 9th anterior roots, not necessarily including the 7th anterior root, and that the presence of the secretory fibres in the 8th root is often associated with the extreme cases of the posterior arrangement though in other cases shifting down of some fibres from the 7th may occasionally occur. Stimulation of the sympathetic trunk. Another method of determining the origin of the sympathetic fibres is to stimulate the sympathetic trunk. This I have done from above downwards and from below upwards. In these experiments, either urethane was given and the brain destroyed, or the brain and cord destroyed without giving urethane in order to avoid the chance of reflex secretion, but no difference in result was found by the two methods. The sympathetic trunk was exposed,
7 SYMPATHETIC OF TOAD. a spinal nerve was tied, cut peripherally of the ligature and at its exit from the vertebra. The sympathetic was cut and isolated up to the next ganglion. The spinal nerve was then held up and the sympathetic trunk immediately above or below it was stimulated. The spinal nerves and the sympathetic trunk were successively treated in the same way. In five toads the sympathetic was thus stimulated from above downwards beginning between the 3rd and 4th ganglions. The main object of these experiments was to see how far up the chain stimulation would cause secretion in the hind-limb. In two experiments out of five, stimulation above the 4th ganglion caused secretion in the whole extent of the leg and in the foot. In two experiments out of four secretion in the same area was obtained by stimulating above the 5th ganglion. The relative amount of secretion in the thigh and lower leg varied in the different experiments. In the back the secretion began in the region of the peripheral distribution of the nerve immediately below the point stimulated. Stimulation at lower levels caused secretion in the whole of the dorsal surface of the limb in all cases, but the secretion varied considerably in amount. In the series in which the sympathetic was stimulated from below upwards the object was to determine the lowest part capable of causing secretion in the fore-limb and head. Experiments were made on four toads, beginning the stimulation below the 5th ganglion. The lowest part from which secretion in the head was obtained was below the 4th ganglion. It was obtained in one case only and it was a slight secretion in one side of the head. Stimulation below the 3rd ganglion in two cases caused secretion in the lower half of the head and some in the fore-limb. Stimulation below the 2nd ganglion caused copious secretion in both head and fore-limb. In one case there was a good secretion on the skin of the lower jaw and in the skin of the flexor side of the fore-limb. The range of innervation in these experiments conforms closely to that found in those in which the spinal nerves inside the vertebral canal were stimulated. But in stimulating the sympathetic trunk there is some risk of the current spreading to the pre-ganglionic fibres of the neighbouring root. Whilst I do not think this occurred in my experiments I have no objective evidence of this to offer. Finally I may mention that I have stimulated the peripheral ends of the dorsal cutaneous nerves of the trunk and find that there is little or no overlapping of their secretory area, i.e. of the areas of the postganglionic fibres running to the trunk by the successive spinal nerves. PH. LVI1. 24: 365
8 366 K. UYENO. SUMMARY. The origin from the spinal cord of the secretory fibres of the skin glands of the toad recently described by E. J. Bruicke was investigated. As found by B ruick e the 2nd to 7th nerves constantly contain secretory fibres, but the 8th nerve does not always cpntain them. When it does there is generally an extreme posterior arrangement of the anterior roots in the region of the lumbar plexus. The 9th nerve has no secretory fibres. The overlapping of the areas of skin supplied by the successive nerves is great. Any given portion of the skin of the back is normally innervated by three spinal nerves; the skin of the hind-limb may be innervated by all the nerves from the 3rd to the 8th. The 3rd and 4th nerves send secretory fibres both to the fore and hind limb. The areas actually found to be affected were often less than here given; this is attributed to varying loss of excitability caused by loss of blood. The general plan of arrangement of the sympathetic secretory fibres of the toad conforms to the plan given by Langley and Orbeli and by Langley for other sympathetic fibres in amphibia. I am greatly indebted to Prof. Langley for his kind suggestions and advice during the course of this experiment. REFERENCES. (1) Langley and Orbeli. This Journ. 41, p (2) Langley. Ibid. 41, p (3) Langley and Orbeli. Ibid. 42, p (4) Briicke. Ztsch. f. Biol. 74, p
products2. Clearly, if similar results to those obtained by Ginezinsky
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