Print version ISSN 1019-9128
J. S. Afr. Vet. Assoc. vol.82 no.3 Pretoria Sept. 2011
M A Martinez-PereiraI,*; E M RickesII
INeuroscience Post-graduate Program and Comparative Neurobiology Laboratory, Physiology Department, Health Basic Science Institute, Federal University of Rio Grande do Sul, Rua Sarmento Leite, 500, Porto Alegre, RS, Brazil, 90046-900
IIParasitology Post-graduate Programme, Biology Institute, Federal University of Pelotas, Rio Grande do Sul, Brazil
In this study, the spinal nerves that constitute the lumbosacral plexus (plexus lumbosacrales) (LSP) and its distribution in Chinchilla lanigera were investigated. Ten chinchillas (6 males and 4 females) were used in this research. The spinal nerves that constitute the LSP were dissected and the distribution of pelvic limb nerves originating from the plexus was examined. The iliohypogastric nerve arose from L1 and L2, giving rise to the cranial and caudal nerves, and the ilioinguinal nerve arose from L3. The other branch of L3 gave rise to the genitofemoral nerve and 1 branch from L4 gave rise to the lateral cutaneous femoral nerve. The trunk formed by the union of L4-5 divided into medial (femoral nerve) and lateral branches (obturator nerve). It was found that the LSP was formed by all the ventral branches of L4 at L6 and S1 at S3. At the caudal part of the plexus, a thick branch, the ischiadic plexus, was formed by contributions from L5-6 and S1. This root gave rise to the nerve branches which were disseminated to the posterior limb (cranial and caudal gluteal nerves, caudal cutaneous femoral nerve and ischiadic nerve). The ischiadic nerve divided into the caudal cutaneous surae, lateral cutaneous surae, common fibular and tibial nerve. The pudendal nerve arose from S1-2 and the other branch of S2 and S3 formed the rectal caudal nerve. The results showed that the origins and distribution of spinal nerves that constitute the LSP of chinchillas were similar to those of a few rodents and other mammals.
Keywords: anatomy, Chinchilla lanigera, lumbosacral plexus, pelvic limb innervation, posterior limb.
The order Rodentia includes approximately 40 % of described mammal species2. Among these, some are of great interest in commercial breeding, like the chinchilla (Chinchilla lanigera, Hystricomorpha, Chinchillidae)6. Owing to indiscriminate hunting throughout the 19th century these animals were considered extinct23,24. However, the unique characteristics of the coat (30 times softer than human hair and of high density, about 20 000 pili/cm2) were the motive for the initial breeding of this species in captivity. Currently, the state of Rio Grande do Sul represents the largest breeder and exporter of chinchilla skins in Brazil, but the national market is growing, mainly in pet animals. Chinchillas are bred for the same purposes in other countries30,31. In spite of its commercial importance and its recent inclusion among animals bred as pets, there is a lack of studies related to its biology.
The spinal origins of the lumbosacral plexus (LSP) that supply the posterior limb have been studied in variety of mammals including the rat1,11,22,35, mouse12, guinea pig13, rabbit 5,21,26, Brazilian rock cavy25, agouti29, porcupine3,4, South American fur seal9, dog19,28 and cat14,20. In the chinchilla, the brachial plexus10,18, the formation of the hepatic portal vein7, the morphology of the digestive system8 and the organisation, distribution and supply area of the middle cerebral artery15 have been studied. However, to the author's knowledge this is the first study on the spinal origins and distribution of the areas innervated by the LSP in Chinchilla lanigera. The purpose of this study was to document the spinal nerves that constitute the LSP and supply the posterior limb in this species.
MATERIALS AND METHODS
Ten chinchillas (6 males and 4 females) that were sacrificed at breeding farms in Pelotas city, Brazil, were used. The abdominal cavity was opened by an incision along the linea alba and dissection of the abdominal muscles. The pelvic symphysis was cut with rib cutters and the pelvic cavity was opened. The organs of the abdominal and pelvic cavities were removed without the spinal nerves constituting the LSP. The quadratus lumborum, psoas minor and psoas major muscles were dissected carefully. The ventral part of the lumbar and sacral vertebral bodies and the area from the last thoracic vertebra to the end of sacrum was completely exposed. The origins of spinal nerves that constitute the LSP and the supply of the nerve branches that originate in this plexus in both posterior limbs were examined. The best visualisation of the nerve structures was obtained with a solution of 30 % glacial acetic acid diluted in absolute ethanol for 30 minutes33. Subsequently, the dissections were fixed in 10 % formaldehyde aqueous solution and photographed. The terminology is according to the Nomina anatomica veterinaria40.
Lumbosacral plexus formation
It was observed that the ventral branches of L4 to L6and S1 to S3 spinal nerves formed the LSP, innervating the pelvic limb and the abdominal, inguinal, perineal and perianal regions in the chinchilla (Fig. 1). Five nerves originating in the lumbar plexus of the chinchilla had been formed from only 1 ventral spinal branch. The ventral branch of L1 and L2 formed the cranial and the caudal iliohypogastric nerves, respectively (Fig. 1). One branch from L3 gave rise to the ilioinguinal nerve and other branch of this spinal root formed the genitofemoral nerve (Fig. 1). One branch from L4 gave rise to the lateral cutaneous femoral nerve (Fig. 1). After joining the branch from L4,L5 divided into medial and lateral branches. The medial branch formed the femoral nerve, while the lateral branch formed the obturator nerve (Fig. 1). A common root was formed distally from a branch from L5, the entire L6 and a branch from S1 (Fig. 1). This root gave rise to the ischiadic plexus (cranial and caudal gluteal nerves, caudal cutaneous femoral nerve and ischiadic nerve), branches of which were scattered throughout the posterior limb (Fig. 2). After giving off the 1st branch to form the ischiadic plexus, S1 merged with S2 to form the pudendal nerve (Fig. 1), while the other branch of S2 joined S3 to form the rectal caudal nerve (Fig. 1). However, in 3 animals, S3 did not participate in the composition of this root.
Lumbosacral plexus nerve distribution
The cranial iliohypogastric nerve emerged between the psoas major and minor muscles and divided into 3, forming the medial, intermediate and lateral branches at the medial side of the abdominal wall and peritoneum (Fig. 1). The caudal iliohypogastric nerve supplied the paralumbal fossa, craniolateral part of the femur and the ventral abdominal wall (Fig. 1).
The ilioinguinal and the genitofemoral nerves, after emerging between the lumbar muscles, continued subperitoneally and in a caudo-ventral direction towards the annulus inguinalis abdominalis (Fig. 1). These nerves innervated the internal abdominal oblique muscle and the cremaster muscle, the testicular fascia, spermatic funiculus and prepuce in males, the teats in females and the skin of the medial side of the femoral region in both sexes.
The lateral cutaneous femoral nerve (Fig. 1) arose from the LSP, reaching the caudal iliac region by crossing the abdominal muscles. It extended over the external abdominal oblique, iliac and tensor fasciae latae muscles, the skin of the femoral region and the craniomedial side of the knee joint.
The femoral nerve originated from the LSP with the obturator nerve (Fig. 1). It was the thickest nerve from the plexus. After emerging between the psoas major and minor muscles and innervating them, together with the deep lumbar muscles, it reached the femoral space running caudo-ventrally and emitting 2 femoral quadriceps muscle branches. The saphenous nerve arose lower down. It divided into 3 branches to the gracilis, pectineus and sartorius muscles and a branch to supply the skin and fascia in the medial femoral region.
The obturator nerve had a similar origin to the femoral nerve. After leaving the pelvic cavity through the obturator foramen, this supplied branches to the adductor, pectineus, gracilis, internal and external obturator muscles.
The ischiadic plexus was a nerve trunk arising from the union of the spinal nerves L5-6 and S1, which supplied the iliac region dorso-caudally and extended caudally in the femoral region. This plexus branched and gave rise to 4 nerves: cranial gluteal, caudal gluteal, caudal cutaneous femoral and ischiadic (Fig. 2). The cranial gluteal nerve (Fig. 2), after leaving the pelvic cavity through the incisura ischiadica major, supplied the branches of the deep gluteus, piriform and tensor fasciae latae muscles. The caudal gluteal nerve (Fig. 2) was a motor nerve arising from the caudal portion of this common trunk and that innervated the superficial gluteus, cranial part of the biceps femoris, abductor cruris caudalis and the vertebral head of semitendinous and semimembranous muscles. The medial gluteal muscle was innervated by the 2 gluteal nerves. The caudal cutaneous femoral nerve (Fig. 2) innervated the biceps femoris and semitendinous muscles and after passing between these muscles, supplied the skin over the tuber ischiadicum, the caudal portion of the femur and by a union with the pudendal nerve, the perineum.
The common trunk continued as the ischiadic nerve after giving rise to the caudal cutaneous femoral nerve (Fig. 2). The ischiadic nerve branched into the proximal muscular branch for the internal obturator, gemelli and quadratus femori muscles. This branch extends to the skin after innervating the caudal portion of the biceps femoris, semitendinous and semimembranous muscles. Near the knee joint, the ischiadic nerve divided into the caudal cutaneous surae, lateral cutaneous surae, common fibular and tibial nerve. The cutaneous surae lateralis nerve (Fig. 2), first branch of the ischiadic nerve innervated the subcutaneous tissue and skin in the cranial surae region, while the caudal cutaneous surae nerve crossed the caudal sural region and innervated the skin of this region and the common calcaneal tendon (Fig. 2). The tibial nerve (Fig. 2) ran to the level of the tarsal joint, giving off slender branches to the skin in this region, and divided into the dorsal digital and common plantar nerve V. After this branch, the tibial nerve gave off a distal muscular branch that extended to the flexor muscles, ran between the 2 heads of the gastrocnemius and popliteus muscles, continued as branches to the muscles of the plantar surface of the metatarsus and divided into the common plantar digital nerves II, III and IV. The common fibular nerve (Fig. 2) passed over the gastrocnemius muscle and entered the sulcus between the peroneus longus and extensor digitorium lateralis muscles, then dividing into the superficial fibular and profound fibular nerves. The superficial fibular nerve innervated the skin of the dorsum of the tarsus and metatarsus and emitted the muscular branches to the cranial tibial, extensor digitalis longus and extensor digitalis lateralis muscles, and formed the common dorsal digital III and IV nerves. The deep fibular nerve innervated the fibularis longus and fibularis brevis muscles.
The pudendal nerve (Fig. 1) crossed towards the caudal pelvic aperture where it divided into the dorsal nerves of the penis or clitoris and the superficial and deep perineal nerves. The first innervated the ischiocavernosous, bulbospongiosous and retractor penis muscles and the prepuce in male and the constrictor vulvae muscle, clitoris and vulva in female. The superficial and deep pudendal nerves innervated the skin and muscles of the anal and perianal regions.
The rectal caudal nerve (Fig. 1) innervated the region up to the end of the rectum, the sphincter muscles of the anus and the skin of the anal region.
Lumbosacral plexus formation
It has been reported that the LSP was formed by the union of the ventral branches that vary between the L2 to L6 and S1 to S4 spinal nerves in domestic mammals16,19,28,37 and L3 to L5 and S1 spinal nerves in South American fur seal9. In species similar to the chinchilla it was observed that LSP was formed by ventral branches that vary between T13-15,L1 to L7 and S1-3 spinal nerves4,13,22,25,26,29.
In the present study it was found that the LSP was formed by the union of the ventral branches of spinal nerves L4 to L6 and S1 to S3. In terms of the branches that contributed to formation of the LSP (invariably the last 3 lumbar spinal nerves and the 1st 3 sacral nerves), the LSP in the chinchilla is close to that of the cat19, guinea pig13, rabbit26, Brazilian rock cavy25 and South American fur seal9.
However, the number of the spinal nerves was not the same owing to the different number of vertebrae in each species. The LSP formation was totally different from those reported for the rat22, agouti29 and porcupine4.
A common nerve root was found in the LPS that gives rise to the nerves innervating the posterior limbs of the chinchilla, which in the present study is referred to as the ischiadic plexus, according to the nomenclature used by Schwarze and Schröder36. We chose this name because this constitutes a common root, originating from different spinal nerves and that forming a common trunk that branches into nerves: the cranial gluteal, caudal gluteal, caudal cutaneous femoral and ischiadic. A common root has been reported in ruminants19, dogs19,28, humans17, cats19,20 and South American fur seals9. However, the term ischiadic plexus was used only in the South American fur seal.
There are many reports giving the data about the formation of this common root in rodents. In the Brazilian rock cavy25 it was reported that L5-6 or L6-7 and S1 contribute to formation of the common root, while in the agouti29 in some cases L4-5 contribute with L6-7 and S1 to the common root. However, in porcupines4 the common root consisted of the entire L4 and S1 and a slender branch from S2 and L3. Two descriptions were found for the rat. Asato et al.1 reported that L4 and L5 always and L6 rarely contribute to formation of the common root. On the other hand, other authors stated that L4-6 and S1-2 contribute to formation of the common root in rats22,35,39. However, in the LSP of the chinchilla this common root was formed by L5-6 and S1 which was consistent with what has been described in the rabbit26, agouti29 and Brazilian rock cavy25, but not in other rodents1,4,13,22,35,39 and some mammals, including humans 9,17,19,28,37.
Lumbosacral plexus nerve distribution
The formation of the iliohypogastric and ilioinguinal nerves in various domestic mammals has been described as follows: in species that have 6 lumbar vertebrae (herbivores), the iliohypogastric nerve arises from the ventral branch of L1 and the ilioinguinal nerve arises from L216,19,37 . Species that have 7 lumbar vertebrae (carnivores) have 2 iliohypogastric nerves, cranial and caudal, which arise from the ventral branches of L1 and L2, and the ilioinguinal nerve, which arises from the ventral branch of L316,19,28,37. However, the chinchilla has 6 lumbar vertebrae, but L1 and L2 give rise to the cranial and caudal iliohypogastric nerves and the ilioinguinal nerve arises from L3. In all the studies it was reported that these 2 nerves innervate the same regions. Therefore, these results were different from those obtained for other rodents3,4,13,22 and the South American fur seal9.
The formation of the genitofemoral and lateral cutaneous femoral nerves in the chinchilla was similar to that of sheep, goats19 and South American fur seals9 in terms of common origin, while it was completely different from all other animals in its origin from L3 and L4 3,4,13,19,26,28. However, a common origin of the genitofemoral nerve formed by part of L3 and L4 joining the common trunk of the obturator and femoral nerves, as described in South American fur seals9, was not observed.
The formation of the femoral and obturator nerves from the same spinal nerves in the chinchilla was similar to that reported in rats22, agouti29, Brazilian rock cavy25, porcupine3,4 and other mammals9,19,28. However, this study detected that both nerves originated from L4 and L5, which differs from previous reports, only being similar to 1 of the types described in the Brazilian rock cavy25. The 1st branch arising from the femoral nerve supplied the medial muscles of the femur, while the 2nd branch, the saphenous nerve, innervating the skin and muscles of the posterior limb, extended over the skin of the medial part of the posterior limb in rats22,39, guinea pigs13 and rabbits26.
Although it has already been discussed, an examination of the formation of the ischiadic plexus was necessary to observe the root and the areas of innervation of the cranial gluteal, caudal gluteal, caudal cutaneous femoral and ischiadic nerves individually. Since the literature records different origins for these nerves, the variations are discussed.
In the Brazilian rock cavy the cranial gluteal and the caudal gluteal nerves were described as branches originating from the ischiadic nerve, without considering the formation or existence of the ischiadic plexus25,34. Similar descriptions of both gluteal nerves were given for the cat and the dog, where these were considered to be branches of the final portion of the LSP or branches of the ischiadic nerve19,28. In some rodents the gluteal nerves originated individually from the spinal nerves that constitute the LSP3,4,13,22, but in rats the caudal gluteal nerve is a branch of the perineal nerve22.
The caudal cutaneous femoral nerve in guinea pigs was reported to originate from the LSP with the ischiadic nerve and then to separate from it; in porcupines this nerve arises from the common root with the cranial gluteal, caudal gluteal and ischiadic nerves3,4 and the presence of this nerve was not mentioned in the Brazilian rock cavy 25,34 or agouti29.
Like the variation of the lumbar and sacral vertebrae, the nerve roots that form the ischiadic nerve, proved to be distinct for different species but it could be noted that they represent the last spinal nerves forming the LSP1,3,4,13,19,20,22,25,26,28,29,34,35,38. The ischiadic nerve, after giving off the caudal cutaneous surae nerve divided equally into the common fibular and tibial nerves observed in rodents1,3,13,22,25,29,34,35as, rabbits26 and other mammals 9,16,19,20,28,37,38.
Despite varying information about the origins of these nerves, the innervation areas of the chinchilla were similar to those of rodents1,3,13,22,25,29,34,35, rabbits26 and other mammals cited16,19,20,28,37,38. However, the results presented in this study show that the cranial gluteal, caudal gluteal, caudal cutaneous femoral and ischiadic nerves arise from a common trunk, the ischiadic plexus, which branches out to innervate the posterior limb, consistent with observations from South American fur seals9.
In this study, the pudendal nerve arose from S1-2 and the rectal caudal nerve originated from S2-3. These results differ from all previous descriptions of the origin of these nerves in guinea pigs13 and rabbits26. Neither the formation of the pudendal plexus22 nor the presence of a common trunk formed by L5-S1 as described in rats27,32 was observed in chinchillas. The common emergence of both nerves was similar only to that described in cats19,20, dogs19,28, South American fur seals9 and, probably in Brazilian rock cavy25 and porcupines3,4. In the chinchilla the pudendal nerve was divided into a superficial and deep perineal nerve as in dogs19,28.
In conclusion, the formation of the LSP in the chinchilla was partly consistent with the plexus in the guinea pig and Brazilian rock cavy, rabbits and South American fur seals, and differs from all other species discussed. The formation of the common root of the nerves that innervate the posterior limb bore a slight similarity to rabbits, agouti and Brazilian rock cavy, while it was significantly different from the remaining rodents and other mammals discussed. The authors of this study also evaluated the formation of the nerves originating from the LSP in the chinchilla and came to the following conclusions: the iliohypogastric nerve was present and consisted of cranial and caudal nerves; the ischiadic plexus was present and formed a common root that innervated the posterior limb and gave rise to the cranial and caudal gluteal, caudal cutaneous femoral and ischiadic nerves; the ischiadic nerve divided into the lateral cutaneous surae, caudal cutaneous surae, common fibular and tibial nerves; the pudendal nerve divided into 3 nerves, namely the dorsal penis (male) or clitoris (female), superficial and deep perineal nerves. Knowing the distribution of the ischiadic nerve in chinchilla enables delimitation of a safe area for intramuscular application of drugs, namely the semi-membranous muscle region or even the caudal face of the semitendinous muscle. The data presented are similar to those reported previously in rodents and other mammals, but some characteristics were shown to be peculiar to the chinchilla.
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Received: May 2010.
Accepted: June 2011.