THE AFFERENT INNERVATION OF THE KIDNEY AND TESTIS OF TOAD
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1 THE AFFERENT INNERVATION OF THE KIDNEY AND TESTIS OF TOAD AKIRA NIIJIMA* Department of Physiology, Niigata University School of Medicine, Niigata Afferent impulses were recorded by Tower (1) from ramus communicans VI and VII of the frog's sympathetic nerve trunks when mechanical stimuli were applied to the kidney and testis. It is a common phenomenon that severe pain is felt at the crisis of nephrolithiasis. McLellan and Goodell (2) reported a case in which pain referred to the costovertebral angle was caused by mechanical distension of the pelvis of a kidney. The existence of sensory receptors in the kidney which cause pain traveling over the sympathetic system is certain, but little is known about the pattern of impulses from these sensory fibers. The present paper will mainly deal with the mechanism of visceral sensation from kidney and testis of toad. METHOD All experiments were performed on toads. Usually, in toads, 4 nerve trunks from sympathetic chains supply each side of kidney and testis as shown in fig. 1. These nerve trunks were freed from the surrounding tissues and cut as far centrally as possible, thus enabling the potential recording of the action current from these trunks. Kidneys and testis were removed from their beds with nerves as a whole, thus the kidney-testis-nerve preparation was made (fig. 1). In some preparations the single nerve fibers were dissected from trunks with the aid of a binocular microscope ( ~60) by the technique described by Kato (3) and Tasaki (4). For mechanical stimulation, an apparatus was used which was schematically shown in fig. 2. The air was compressed by the pump P and charged into the reservoir R, then the cock C was turned to the tambour T. The compressed air streamed into the tambour, so that the tambour swelled up and the rod connected to it was pulled downward, thus the kidney-testis preparation was given pressure stimuli by a plastic plate (2 ~2mm.2) which was connected at the terminal of the rod. Then the cock C was turned outward, the air in the tambour flowed out, then the tambour collapsed, suspending the stimuli. The strength of the pressure stimulus given to the testis or kidneys was controlled by a Hg-manometer as shown in fig. 2. The dimension of receptive field supplied with a nerve trunk or a single Received for publication December 20, 1958.
2 240 A. NIIJIMA FIG. 1 FIG. 2 FIG. 1. Schematic representation of sympathetic innervation of kidney and testis. S:Sympathetic chain. K:Kidney. T:Testis. N1, N2, N3, N4:Nerve trunks from sympathetic chain to kidney and testis. FIG. 2. Diagramatic representation of apparatus used for mechanical stimulation of kidney and testis. P:Pump. R:Reservoir of compressed air. C:3-way cock connected to reservoir and tambour. T:Tambour and rod with small plastic plate at its end. Pr:Preparation with nerve. M:Hg-manometer. S:Loud-speaker. afferent fiber to the mechanical stimuli was measured by the stimuli of von Frey's hair. The action potentials were led off through silver, silver-chrolide electrodes to a condensor-coupled amplifier and oscilloscope with the Grass type long recording camera. RESULTS Afferent impulses from kidneys and testis:four nerve trunks from sympathetic chains supplying each side of kidneys and testis will be named conventionally N1, N2, N3 and N4 from cranial to caudal as shown in fig. 1. Diameter of each of these nerve trunks was about 100ƒÊ including the surrounding tissues. When light mechanical stimuli were applied continuously to the kidney, several afferent impulses were elicited from these nerves at the onset of pressure stimulus. If the stimulus-strength was increased, more frequent afferent impulses were elicited not only at the moment of onset of stimulus but also several seconds after that. These impulses could be classified into several groups according to their spike-height and their trend in adaptation. Generally, it may be true that the impulses of large spikes belong to relatively slowly adapting type and impulses of small spikes to more slowly adapting elements. The rapidly adapting
3 INNERVATION OF KIDNEY AND TESTIS 241 impulses with the large spike amplitude such as elicited from touch receptors in the skin could not be found (fig. 3). FIG. 3. Afferent impulses from a right nerve N2 during sustained pressure on cranial region of right kidney. Intensity of pressure, 5mmHg/2 ~2mm.2 in A, 10mmHg/2 ~2mm.2 in B. The horizontal line represents 1sec. On stimulating the testis by the same apparatus, almost the same results were obtained. Distribution of receptors:records taken from a right side nerve N1 showed that the cranial part of the right kidney was more sensitive than the middle part of that to mechanical stimuli, the caudal part of right kidney and all parts of left kidney were proved without effect (fig. 4). FIG. 4. Afferent impulses from a right nerve Ni during sustained pressure on cranial, middle and caudal region of right kidney. Shaded areas show the sensitive parts to pressure stimulus. The horizontal line represents 1sec.
4 242 A. NIIJIMA Seeing from the pattern of these spike potentials it may be true that there are not so many afferent fibers in this nerve as in the other nerve trunks innervating stomach, intestine, pancreas, mesentery etc. Pressure stimuli given to the testis showed almost the same effects. If the records taken from the right side nerve N2, the middle parts of the kidney and testis of the right side were most sensitive. Fig. 5 shows the relative sensitivity of the kidney and testis to the mechanical stimuli estimated by the records taken from both side of N1, N2, N3 and N4. From these facts it may be said that the surfaces of the kidney and testis are supplied segmentally with afferent nerves of sympathetic nerves as shown in fig. 5. Further afferent impulses could be recorded from splanchnic nerve by mechanical stimuli to the cranial part of the kidney. FIG. 5. Schematic diagram of sensitivity to mechanical stimuli of kidney and testis estimated by the records taken from both side of N1, N2, N3 and N4. Shaded areas show the sensitive parts to pressure stimulus. FIG. 6. Impulses in a single afferent fiber from kidney during sustained pressure on this organ. Diameter of this fiber is about 5ƒÊ. Intensity of pressure, 10mmHg/2 ~2mm.2 in A, 20mmHg/2 ~2mm.2 in B, 30mm ~2mm.2 in C. Shaded area shows the sensitive part to pressure stimulus. The horizontal line represents 1 sec.
5 INNERVATION OF KIDNEY AND TESTIS 243 Observations on single fiber preparations:a single myelinated afferent fiber with diameter of about 5ƒÊ could be dissected from the right side nerve N2. Afferent impulses were elicited from this fiber by mechanical stimuli to the right kidney. When light stimuli were applied continuously to the kidney, a few impulses were observed at the onset of the stimuli. With stronger stimuli more frequent impulses were elicited not only at the beginning but also several seconds after the onset of the stimuli. From these facts it seems clear that these impulses were elicited from relatively slowly adapting mechano-receptors. The dimension of the receptive field to mechanical stimuli in this single afferent fiber was about 5 ~5mm.2 on the surface of kidney (fig. 6). A single afferent fiber from the testis with diameter of 5ƒÊ showed also the same pattern of impulses (fig. 7). FIG. 7. Impulses in a single afferent fiber from testis during sustained pressure on this organ. Diameter of this fiber is 5ƒÊ. Shaded area shows the sensitive part to stimulus. The horizontal line represents 1sec. The existence of smaller afferent fibers were speculated by afferent impulses from nerve trunks, but these could not be dissected because of technical difficulties. DISCUSSION From the above-mentioned facts it is obvious that the kidney and testis of the toad are supplied with afferent fibers contained in sympathetic trunks. One of the largest fibers of them is about 5 p in diameter and it is probably true that this fiber belongs to the smaller group of Gasser's 'A'-class. The modes of the afferent innervation among kidney, testis and other organs supplied with splanchnic nerves are as follows:1) The digestive organs and mesentery are supplied with splanchnic fibers in a overlapped manner (5). 2) The surface of the kidney and testis are supplied segmentally with afferent fibers of sympathetic nerves (fig. 5). 3) The receptive field of kidney and testis to mechanical stimuli supplied with a single afferent fiber is far smaller than that of splanchnic afferent fiber. The receptive field of kidney and testis
6 244 A. NIIJIMA supplied with a single afferent fiber is usually about 5 ~5mm.2, and that of a single splanchnic nerve fiber is often larger than 10 ~10mm.2. Tower (1) reported that the kidney and testis were supplied with rapidly adapting receptors. But from above-mentioned facts it may be speculated that the adaptation of the mechano-receptors of the kidney and testis is relatively rapid compared with slowly adapting receptors in the skin, however, it is slower than that of rapidly adapting touch receptors in the skin. Recently, the frog skin mechano-receptors have been classified into four types by Catton (6). According to him, mechanoreceptors of the kidney and testis mainly belong to the type (b) i.e. slowly adapting touch receptor or to the category 'A' of Fessard and Segers (7). Further, small and more slowly adapting impulses were sometimes observed. They were probably due to non-myelinated axons. These impulses may be elicited from the receptors which belong to the type (d) in Catton's classification or to 'pain' ending of Fessard and Segers. When the peritoneal covering of the kidney and testis were removed, no afferent impulses were observed at all. From these facts it may be concluded that mechano-receptors of kidney and testis are mainly located on the peritoneal surfaces of these organs. It is open to question, however, whether these afferent impulses from mechanoreceptors have any definite reflex effects or not. SUMMARY The afferent impulses from the nerve trunk or a single nerve fiber to the kidney and testis of toad due to mechanical stimuli have been studied by means of oscilloscopic recording. 1) Kidney and testis are innervated segmentally with sympathetic trunks from cranial to caudal. 2) The receptive field of a single afferent fiber of these nerves is far smaller (5 ~5mm.2) than that of splanchnic nerve fibers (10 ~10mm.2). 3) The adaptation of these receptors is relatively, at times, extremely slow. The former probably belongs to the type (b) in Catton's classification or to category of type 'A' endings of Fessard and Segers, and the latter seems to belong to the type (d) in Catton's classification or to category of 'pain' endings of Fessard and Segers. REFERENCES 1. TOWER, S. Action potential in sympathetic nerves, elicited by stimulation of frog's viscera. J. Physiol. 78: , MCLELLAN, A. M. AND GOODELL, H. Pain from the bladder, ureter and kidney pelvis. Res. Publ. Ass. nerv. ment. Dis. 23: , KATO, G. The microphysiology of nerve. Tokyo: Maruzen, TASAKI, I. Nervous transmission. Springfield, Illinois: Charles C Thomas, NIIJIMA, A. On the multiple sensory innervation of viscera (Japanese). Seitai no Kagaku (Medical Science) 9: , CATTON, W. T. Some properties of frog skin mechano-receptors. J. Physiol. 141: , FESSARD, A. AND SEGERS, M. Quelques caracteres differentiels des recepteurs cutanes de la Grenouille. C. R. Soc. Biol., Paris, 137: , 1943.
AFFERENT IMPULSES FROM SINGLE MYELINATED FIBERS IN SPLANCHNIC NERVES, ELICITED BY MECHANICAL STIMULATION OF TOAD'S VISCERA
AFFERENT IMPULSES FROM SINGLE MYELINATED FIBERS IN SPLANCHNIC NERVES, ELICITED BY MECHANICAL STIMULATION OF TOAD'S VISCERA AKIRA NIIJIMA Department Physiology, Niigata University School Medicine, Niigata
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