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The Innervation of the Upper Urinary Tract J J. Anat. (1970), 106, 1, pp. 51-61 51 With 12 figures Printed in Great Britain The innervation of the upper urinary tract J. A. GOSLING Department of Anatomy, University of Manchester, Manchester 13 (Received 31 January 1969) INTRODUCTION Although there is general agreement about the extrinsic innervation of the wall of the upper urinary tract, a review of the literature reveals a lack of such unanimity about the intramural distribution of the nerves. Engelmann (1869) described ureteric nerve trunks which branched in the connective tissue surrounding the ureter and formed a rich nerve network. He was unable to detect any free nerve endings in muscle and described nerves continuing on through the muscle coat into the sub- mucosa. These results contrast with those of others who described a variety of nerve endings associated with muscle cells in the renal pelvis and ureter. Many authors have identified nerves in the submucosa, indeed both Engelmann (1869) and Pieper (1951) described nerves extending between cells forming the epithelial lining of the ureter. As indicated by Gruber (1933), very few studies on the detailed intrinsic innervation of the renal caliceal wall appear in the literature and only De Muylder (1952) has attempted to correlate the intrinsic caliceal and renal innervation. In addition, many conflicting opinions have been expressed concerning the existence, type, number and position of intra-mural neurons in the upper urinary tract. The lack of agreement evident in descriptions of nervous tissue elements in the upper urinary tract suggested the present study. MATERIALS AND METHODS The tissues used in this investigation were obtained from freshly killed animals, including 12 monkeys, 16 rabbits, 10 guinea pigs, 10 cats and 7 rats. The rats were killed by an overdose of chloroform vapour, whilst all the other animals were given a lethal intraperitoneal or intravenous dose of sodium pentobarbitone ('Nembutal'). Human material was obtained from 10 post-mortem specimens and 3 specimens removed at operation. The method offixation varied according to the subsequent investigations which were to be performed on the particular tissue, but rapid fixation was sought in every case. Fixed and unfixed tissues were orientated as required and sections varying in thickness between 25 and 100 ,um cut on a freezing microtome. Some specimens were cut longitudinally and opened out in order that serial sections could be prepared in a plane parallel to the wall. The techniques used in this investigation were the osmium tetroxide method of Champy (1913), Coles's (1950) modification of the gold chloride method, Rintoul's (1960) modification of the Bielschowsky-Gros silver technique and Gomori's modification of the Koelle & Friedenwald technique for tissue cholinesterases 4-2 52 J. A. GOSLING (Pearse, 1960). Using the latter technique, specimens from recently removed tissues were fixed in a formalin-sucrose ammonia solution (Pearson, 1963) for 2-8 h. Following fixation, frozen sections were cut and washed briefly in de-ionized water before being placed in the incubating medium at 37 'C. Acetyl thiocholine iodide was most often used as the substrate, although butyryl thiocholine iodine was occasion- ally used as an alternative. As controls, some sections from each of the tissues were stained for reticular fibres, elastic and connective tissue. RESULTS The intrinsic innervation of the regions mentioned was found to have basic simi- larities irrespective of the species of animal used, and unless otherwise stated the following descriptions apply to all the species examined. Nerves approach the region by two routes; some travel along the tunica adventitia of the vessels of supply (Fig. 1), whilst others run singly or in groups through the loose connective tissue adjacent to the urinary tract (Fig. 2). Some nerve bundles become detached from the vessels as they reach the renal pelvis or ureter (Fig. 3); others, at first unassociated with vessels, run for part of their course alongside the arteries before some oftheir branches leave the vessels to enter the nerve plexuses in the wall ofthe region. A number ofthe nerves which remain close to thearteries apparently follow these vessels into the wall of the urinary tract. The nerves which lie in the tunica adventitia of the larger arteries supply fasciculi to the branches of the vessels. The nerves which do not accompany the vessels throughout their course give off branches as they lie in the connective tissue surrounding the ureter or renal pelvis. These form a number of longitudinal nerve bundles interconnected by others having an oblique or transverse direction. In this way a wide-meshed plexus (primary plexus) is built up on the outer aspect of the muscle coat of the region (Fig. 4). The branches from this primary plexus are of variable size; small branches unite in the connective tissue external to the muscle coat to form a secondary plexus within the coarser meshwork of the primary plexus (Figs. 5, 6). Nerve bundles of varying diameters run inwards, passing obliquely in the connec- tive tissue separating the muscle fibres (Fig. 7) and join with other similar bundles on the inner aspect of the muscle coat to assist in the formation of a submucosal nerve plexus (Fig. 8). Although the nerves are closely related to the muscle fibres, free nerve endings have not been positively identified, and nerve fibres entering the smooth muscle cells have not been detected. The submucosal plexus is made up of nerves of various sizes. Branches from it extend inwards towards the mucosal lining of the ureter, pelvi-ureteric region and renal pelvis. The larger branches pass obliquely through the submucosal connective tissue, to divide usually in Y- or T-shaped fashion on the inner aspect of the submucosa. These unite with other similar branches to form a network beneath the basement membrane of the epithelial lining of the region (Fig. 9). Nerve fibres could not be identified penetrating the basement membrane or lying between the epithelial cells. No ganglion cells have been seen in the wall of the upper third of the ureter, the pelvi-ureteric region, the renal pelvis and renal calices. Nerves reach the renal calices by extending upwards as a continuation of the wide- Innervation of upper urinary tract 53 meshed plexus in the connective tissue of the renal pelvis. A coarse-meshed nerve plexus is demonstrated in the connective tissue external to the muscle coat of the distal portion of the renal calices, and it encloses a finer secondary plexus. In the I AV X .1 Jl' .. I7 500 I m I M 1 rs Fig. 1. A longitudinal section through the upper third of the rabbit ureter showing nerves (arrowed) accompanying a ureteric vessel. Cholinesterase activity is also apparent in ureteric smooth muscle (M) and in submucosal nerves (P). Fig. 2. A large nerve branching in the outer part of the fibrous coat of the monkey ureter. Gold chloride preparation. 54 J. A. GOSLING remainder of each calix the nerve bundles forming this coarse plexus become less evident as the kidney is approached until only the constituent fibres of the secondary plexus are demonstrated. *rn li .,. I I) f t : 'M, It ;% .i e.%ve^. 500gI m I . 4 Fig. 3. In this cholinesterase preparation of rabbit ureter two nerves are seen to leave a vessel (surrounded by a nerve network) and pass towards the ureteric muscle coat (M). Fig. 4. This longitudinal section passes slightly obliquely through the fibrous and muscle coats (the latter is seen on the right of the photomicrograph). A large nerve (arrowed) and some of its branches form a wide-meshed 'primary plexus'. Cholinesterase preparation of feline ureter. Innervation of upper urinary tract 55 The nerves forming the submucosal plexus decrease in the caliceal wall and dis- appear in the region in which the epithelial lining of the caliceal fornix is reflected onto the base of the renal papilla. No techniques used in this investigation revealed nerve fibres at the point of attachment of the calix to the renal connective tissue (fig. 10). ..... _ i g ^ ^ X r: :,;, s r;;:: : U ,, - -sst|__.ui..,++.0s:K.<,,sr.jl*}>S;bg,:__.N',$,'eS,^XtjzzLjf#- Fig. 5. Constituent nerves of 'primary' and 'secondary' plexuses seen in an osmium tetroxide preparation of rabbit ureter. Fig. 6. Higher power view of cholinesterase positive nerves of the 'secondary' plexus in human ureter. 56 J. A. GOSLING Nerves supplying the kidney enter the renal parenchyma in association with the major renal vessels. These nerves and their branches often pass in close relationship to the forniceal region of a calix (Fig. 11), but the present study revealed no branches p's..r .........¢:$ i:n ,) . ,.., x;zM -,..........., 48-*f'* 9t;'9 =, z $dF,y,,FI:.3.,j- § *;,> 'i'* e}e~~~4 $ VWeie_:d>l}X;.rt!.jp. .................... .,. K* i31-1..~~~~~~~~~~~~~~~~~~~~~~~~*~~~~~~~~~~vr-4 .,$0.- $, Xj@_s:t-........;.!a;..........., Fig. 7<.B ndes fnrefbe asn btwee mucl cel in th mokeyuee.M dfe Belschowsky-Gros preparation..2 Fig. 8. Nerves of differing sizes close to the muscle coat in the submucosa of the rabbit ureter. Stained using osmium tetroxide.*:,:Yz..:Sw+.:.~~~~~~~~~~~'a f:..,: Innervation of upper urinary tract 57 from these nerves to the caliceal wall; the renal nerves do not separate from the vessels which they accompany. Ganglia containing variable numbers of ganglion cells are found along these nerve trunks in the renal sinus (Fig. 12). ~ ~ Ad L .j. E ,, LOmW I, E 9 C p 300gm L I 10 Fig. 9. Cholinesterase positive nerves forming a nerve network beneath the epithelial lining (E) of the feline ureter. Fig. 10. As the caliceal wall (C) is followed towards its attachment to the renal parenchyma (P) nerves appear to face out in the wall of the renal calix.
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