J. Anat. (1969), 104, 1, pp. 153-159 153 With 4 figures Printed in Great Britain The anatomy of the corpus cavernosum of the bull and its relationship to spiral deviation of the penis

R. R. ASHDOWN* AND J. A. SMITH Department of Veterinary Anatomy, The University, Bristol 2 (Received 10 January 1968) Spiral deviation of the bovine penis occurs at service (Seidel & Foote, 1967) and experiments described by Ashdown & Coombs (1968) suggest that the penis is struc- turally adapted to perform a spiral prescribed by the fibrous architecture of its integument. This paper deals with the structural adaptations of the penis, and supple- ments an account of the penile integument published earlier in thisjournal (Ashdown, Ricketts & Wardley, 1968). It is based on examinations of fresh and preserved specimens from nineteen sexually mature bulls and four new-born calves.

The distal extremity of the The corpus cavernosum penis (c.c.p.) extends to the apex of the bovine penis and is covered by a dense throughout its length. A deep ventral groove houses the and the . Penile tissues are delimited from peripenile tissues in the body of the penis by the outer fibrous coat, but the terminal 10 cm of the organ are covered by the penile integument. The c.c.p. tapers distally to a terminal process about 20 mm in length; the urethral groove becomes shallower, wider, and displaced to the right, housing the urethral process (Fig. 1). Distal to the sigmoid flexure, the tunica albuginea gives rise to the dorsal apical ligament, and terminally it provides the fibrous basis of the terminal swelling ('galea glandis'). The tunica albuginea The tunica albuginea of the corpus cavernosum penis of the adult bull is about 3 mm thick, divisible into an outer longitudinal layer and a thin inner transverse layer. There are connexions between bundles of fibres in each layer, and the longi- tudinal bundles connect with the transverse ones. Fibres of the inner transverse layer pass radially into the cavernous part of the c.c.p. and become continuous with the trabeculae there. These tissues have been described in detail by Preuss (1954). In the region of the dorsal apical ligament this arrangement is modified. Where it is covered by the dorsal apical ligament the thickness of the tunica albuginea is reduced by about 30 %. Figure 2 shows the arrangement of collagen fibres in the tunica albuginea after removal of the dorsal apical ligament. On the left the outer longi- tudinal layer of fibres reaches to the tip of the c.c.p. On the right the outer fibres are at first longitudinal but distally the direction becomes cranio-dorsal and oblique. Ventrally the fibres run longitudinally along the whole length of the urethral groove. * Present address: Department of Anatomy, The Royal Veterinary College, London, N.W. 1. 154 R. R. ASHDOWN AND J. A. SMITH On the dorsal surface of the penis, beneath the dorsal apical ligament, the outer collagen fibres are not arranged longitudinally but instead run obliquely from left caudal to right cranial. On reaching the right side of the penis they interweave with the oblique bundles of fibres which meet them at right angles, so forming a very distinct line of junction. On the dorsal surface of the c.c.p. lateral anastomoses between adjacent bundles of collagen fibres are to a large extent absent, though radial anastomoses are present. In the terminal part of the tunica albuginea, distal to the termination of the dorsal apical ligament, the outer layer of fibres is longi- tudinal over the whole circumference of the c.c.p.

Fig. 1. Ventral view of the distal extremity of the corpus cavernosum penis (c.c.p.) of the bull. The urethral groove is indicated by shading. The ventral extent of origin of the terminal swelling from the tunica albuginea is shown by stippling which extends on to the terminal process of the c.c.p.-the dorsal extent is indicated by a broken line. The base of the free end of the penis is indicated by arrows. The inner transverse layer of fibres, recognizable as far as the apex of the penis, is modified in places. On the dorsal surface the oblique outer fibres, described above, become progressively more transverse in their deeper layers and finally run into the inner trabeculae of the c.c.p. Ventrally, along the sides of the urethral groove, longi- tudinal fibres are found throughout. On the left, in the free end of the penis, the deeper fibres of the inner layer run obliquely from caudo-dorsal to cranio-ventral, becoming longitudinal along the sides of the urethral groove. On the right, the fibres of the inner layer arise in the longitudinal bundles along the right edge of the urethral Corpus cavernosum penis of the bull 155 groove; passing cranio-dorsally they maintain the same direction as the outer layer of fibres in this region and do not become transverse. The structure of the tunica albuginea in the new-born calves was the same as that in the adult bulls.

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Fig. 2. Four views of the distal extremity of the corpus cavernosum penis to show the direction of fibres in the outer layer of the tunica albuginea of the bull. The dorsal apical ligament has been removed and its attachments are shown by the cut ends of its fibres (dorsal and left) and by a broken line (ventral and right). The stippling on the dorsal surface indicates an extensive area of attachment ofthe ligament to the tunica albuginea proximal to the terminal process. The urethral groove is indicated by shading and the base of the free end by arrows. The dorsal apical ligament The dorsal apical ligament is a direct continuation of the outer longitudinal layer of the tunica albuginea. Large bundles of longitudinal fibres arise from the tunica albuginea along the dorsal midline for a distance of 7 cm. The origin then fans out to the left and ventrally, reaching to the distal extremity of the ligament. The fibres of the dorsal apical ligament attach distally to the tunica albuginea; where the c.c.p. abruptly narrows, the ligament blends with the dorsal surface ofthe tunica albuginea. To the right and ventrally the dorsal apical ligament fans out to attach to the tunica albuginea close to the lip of the urethral groove. Except for these attachments (which are shown in Figs. 2 and 3) the ligament is not closely adherent to the underlying tunica albuginea; loose connective tissue occupies the space between the two. 156 R. R. ASHDOWN AND J. A. SMITH The ligament is about 20 cm in length. From a mid-dorsal origin 5 mm in width it fans out to almost completely enclose the c.c.p., and narrows again at its distal extremity (Fig. 3). It can be divided into two fairly distinct parts. The thick part is a strap-like band of dense fibres, longitudinal in direction, and dorsal and left in position. Its average thickness is about 2 5 mm, reaching 3 5 mm half way along its length. On the left the thick part is firmly anchored by its origin from the tunica

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Dorsal Left lateral Right lateral Fig. 3. Four views of the distal extremity of the corpus cavernosum penis of the bull to show the dorsal apical ligament. Thick and thin lines indicate direction of fibres in the thick and thin parts of the ligament respectively. The urethral groove is indicated by shading and the base of the free end by arrows. albuginea; on the right it fans out into the thin part. The fibres of the thin part of the ligament run obliquely, ventrally and to the right, to share with the outer fibrous coat a ventral attachment to the tunica albuginea near the urethral groove. It becomes progressively thinner in its more ventral parts and distally it is pierced by the terminal radicals of the right dorsal artery, vein and nerve. The outer fibrous coat The outer fibrous coat is attached ventrally to the c.c.p. along each side of the urethral groove where some of the longitudinal collagen fibres of the tunica albuginea contribute to it. At the free end of the penis the fibrous tunic divides into two layers which become continuous with the hypodermis of the penile integument and penile Corpus cavernosum penis of the bull 157 sheath. The retractor muscles of the sheath lie in the peripenile fasciae, outside the fibrous coat, and insert on the penile and pre-penile parts of the sheath. There are connexions between the fibrous coat and the dorsal apical ligament along the left edge and on the dorsal surface of the ligament. In the free end of the penis the hypodermis of the penile integument, which is part of the continuation of the outer fibrous coat, is also attached in places to the dorsal apical ligament. Along the ventral edge of the thin part of the dorsal apical ligament the fibrous coat fuses with the ligament. Effect ofspiral deviation on the anatomy of the fibrous structures When the tip of the injected penis is pushed ventrally, the organ bends at the base of the free end of the penis just as it does during spiral deviation. In fresh specimens from which the integumentary structures have been stripped away it is evident that

Fig. 4. Cranial and left lateral view of the distal extremity of the corpus cavernosum penis (c.c.p.) of the bull to show the effect of spiral deviation on the anatomy of the dorsal apical ligament. At the proximal bend in the penis the thick part of the ligament is displaced to the left. At the distal bend the thick part ofthe ligament is stretched across the bent c.c.p. The fibres in the thick and thin parts of the ligament are shown by thick and thin lines respectively and the base of the free end by an arrow. at this bend the thick part of the dorsal apical ligament slips over to the left. As a result, the thin part of the ligament becomes stretched over the dorsal and right lateral surfaces of the penis, and its constituent bundles of fibres become widely separated (Fig. 4). When the tip of the ventrally deviated organ is pushed to the right a second bend forms about 5 cm from the apex and the spiral deviation is complete. At the second bend the fibres of the thick part of the ligament move upwards towards the urethral groove and become tensed across the bend in the penis (Fig. 4). Effect ofremoving the dorsal apical ligament When the dorsal apical ligament is removed from the injected c.c.p. the terminal 10 cm of the organ, previously straight, curves through 450 ventrally and through 450 to the right. The c.c.p. is readily bent into the spiral shape and with the ligament removed the oblique bundles of fibres in the outer layer of the tunica albuginea are seen to be pulled apart from each other when the organ is spiralled. The absence of lateral anastomoses between adjacent bundles becomes very evident. 158 R. R. ASHDOWN AND J. A. SMITH

DISCUSSION The anatomical studies described in this paper reveal two structural adaptations of the bovine penis that allow it to spiral when the penile integument is stretched. First, the collagen fibres of the tunica albuginea of the corpus cavernosum penis in its more distal regions are arranged to allow ventral and right deviation. In the dorsal part of the c.c.p. the tunica albuginea is thinner; its fibre bundles do not freely anastomose and so can be easily pulled apart; and the fibres are oblique in direction. This direction, from caudal and left to cranial and right, is the same as that of the fibres in the dorsal part of the penile integument (Ashdown et al. 1968). The fibres in the right lateral wall of the tunica albuginea, together with the dorsal fibres, make a series ofloops running from caudal and left to cranial and right and these loops permit ventral and right deviation. The oblique fibres in the deep layers of the left lateral wall can also be considered as part of these loops; they do not oppose the deviation. The longitudinal fibres along the urethral groove are ventral in position, directed to the right, and occupy the concave surface of the spiral. Secondly, when spiral deviation commences, the inextensible dorsal apical ligament moves to accommodate to the spiral, as described above. If the dorsal apical ligament is immobilized by sutures the penis is almost completely prevented from spiralling (Ashdown & Coombs, 1968). When the injected penis is manually protruded to stretch the penile integument, the dorsal apical ligament can be felt slipping into place as each of the two bends of the spiral forms. On the other hand, when the dorsal apical ligament is completely removed the injected corpus cavernosum penis takes up a curved shape, deviating ventrally and to the right. Spiral deviation of the penis at service doubles the effective width of the intro- mittent organ (Seidel & Foote, 1967). It is associated with complex anatomical arrangements of the tunica albuginea and the penile integument and probably plays some role in the processes of copulation. Since the penis of the bull does not dilate during , spiralling might significantly increase the tactile stimulus resulting from intromission. SUMMARY 1. The fibrous architecture of the tunica albuginea of the corpus cavernosum penis (c.c.p.) permits deviation ventrally and to the right. 2. Part of the outer longitudinal layer of the tunica albuginea of the c.c.p. is modified to form the dorsal apical ligament. When spiral deviation occurs this liga- ment moves to accommodate its inextensible fibres to the spiral. After removal of the ligament the c.c.p. deviates ventrally and to the right. 3. Spiral deviation of the bovine penis may be functionally significant during the process of copulation. We wish to thank Professor C. W. Ottaway for providing the facilities necessary for this work. Mr G. F. Smith, Chief Veterinary Officer, Milk Marketing Board, gave us much help and encouragement. One of us (J. A. S.) received a research grant from the Veterinary Drug Co. (York) Ltd. Specimens were supplied by Dr H. J. Cembrowicz (Horlicks Farms and Dairies) and Messrs E. J. Simmons and J. W. Stables (Milk Marketing Board). Mr T. Wiltshire drew the illustrations. Corpus cavernosum penis of the bull 159

REFERENCES ASHDOWN, R. R. & COOMBS, M. A. (1968). Experimental studies on spiral deviation of the bovine penis. Vet. Rec. 81, 126-129. ASHDOWN, R. R., RICKETTS, S. W. & WARDLEY, R. D. (1968). The fibrous architecture of the integumen- tary coverings of the bovine penis. J. Anat. 103, 567-572. PREUSS, F. (1954). Die Tunica albuginea penis und ihre Trabekel bei Pferd und Rind. Anat. Anz. 101, 64-83. SEIDEL, G. E. & FOOTE, R. H. (1967). Motion picture analysis of bovine ejaculation. J. Dairy Sci. 50, 970-971.