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International Journal of Morphology

versión On-line ISSN 0717-9502

Int. J. Morphol. v.27 n.3 Temuco sep. 2009

http://dx.doi.org/10.4067/S0717-95022009000300003 

Int. J. Morphol., 27(3):635-642, 2009.

Anatomy of the Nervous of Forearm and Hand of Cebus libidinosus (Rylands, 2000)

 

Anatomía de los Nervios del Antebrazo y Mano de Cebus libidinosus (Rylands, 2000)

*,**Kliver Antonio Marin; ***Frederico Ozanan Carneiro e Silva; *Adryano Augustto Valladão de Carvalho; *,**Guilherme Nobre Lima do Nascimento; *,**Yandra Cássia Lobato do Prado & *Tales Alexandre Aversi-Ferreira

* Neurosciences and Behaviour Primates Laboratory (NECOP) - Federal University of Goiás ­ Goiânia ­ GO - Brazil.

** Institute Atlas of Science and Technology (IACT) ­ Anápolis ­ GO ­ Brazil.

*** Veterinary School ­ Federal University of Uberlândia ­ Uberlândia ­ MG ­ Brazil.

Correspondence to:


SUMMARY: The knowledge on the macroscopic internal structure of Cebus will provide data for histological and biochemical studies and too will contribute to ethological studies. Behavior, memory, use of tools and encephalization index have put the Cebus genus near to chimpanzees in relation to these aspects. The objective of this study is to characterize the nervous model of the forearm and hand of the Cebus monkey. For this, the main nerves and their branches located in the forearm and hand of the Cebus monkey were anatomically characterized, taking into consideration their frequency, number, origin and distribution. The data were compared with the same nerves found in specialized literature in humans, also specialized in other non-human primates. In this study, 7 Cebus libidinosus monkeys were used. The monkeys were provided by IBAMA (Brazilian Institute for the Environment and Renewable Natural Resources), from the city of Sete Lagoas, State of Minas Gerais, in 1970, and housed at the anatomy collection of the Goiás Federal University (UFG). For the nerves of the forearm of Cebus, no variations were observed in the innervation pattern of the muscles, except for the deep flexor muscle of the fingers, which in Cebus and baboons is innervated by the ulnar nerve and in humans and chimpanzees by the median nerve; however, these nerves exchange fibers in the arm and in the brachial plexus. Innervation variations may occur in the fingers of Cebus in relation to other primates, but these variations have been reported with variations in humans. This identical innervation pattern in relation to the nerves of the arm and forearm and hand in Cebus justify its use as model for anthropological evolutionary studies.

KEY WORDS: Capuchin monkey; Cebus; Anatomy; Nerves; Forearm.


RESUMEN: El conocimiento sobre la estructura macroscópica del interior del Cebus proporcionará datos para los estudios histológicos y bioquímicos y también contribuirá a estudios etológicos. El comportamiento, la memoria, el uso de herramientas y el índice del encefalización del género Cebus se plantean en torno a los chimpancés, en relación con estos aspectos. El objetivo de este estudio fue caracterizar el modelo de los nervios del antebrazo y la mano del mono Cebus. Para ello, los principales nervios y sus ramos situados en el antebrazo y la mano se caracterizaron anatómicamente, teniendo en cuenta sus frecuencia, número, origen y distribución. En este estudio se utilizaron 7 monos Cebus libidinosus, todos adultos sanos, con variaciones en tamaño y edad. Los monos fueron suministradas por el Ibama (Instituto Brasileño de Medio Ambiente y los Recursos Naturales Renovables), ciudad de Sete Lagoas, Estado de Minas Gerais, en 1970 de la colección anatómica de la Universidad Federal de Goiás (UFG). En el antebrazo de Cebus no se observaron variaciones en las características de los nervios de los músculos, excepto para el músculo flexor profundo de los dedos, que en Cebus y babuinos, está inervado por el nervio ulnar y en los seres humanos y los chimpancés por el nervio mediano; sin embargo, estas fibras nerviosas cambian en el cuello y en el plexo braquial. Las variaciones de los nervios pueden ocurrir en los dedos de Cebus con respecto a otros primates, pero estos cambios están relacionados con las variaciones que ocurren en los seres humanos. Este patrón similar de los nervios de los nervios del brazo y antebrazo y mano en Cebus, justifica su uso como modelo evolutivo para estudios antropológicos.

PALABRAS CLAVE: Mono capuchino; Cebus; Anatomía; Nervios; Antebrazo.


INTRODUCTION

The Cebus genus features the largest geographical distribution among neotropical primate species, being observed from Colombia and Venezuela all the way to northern Argentina, inhabits tropical, subtropical and riverside forests, as well as savannah and semi-arid regions of Brazil (Lopes, 2004). Cebus present an immense capacity to handle tools for obtaining food and amusement, and such activities are observed both in captivity and in the wild (Breseida & Ottoni, 2001; Resende & Ottoni, 2002). Such aspects justify the choice of the Cebus monkey for anatomical and behavioral studies.

Anatomical studies were conducted on the thoracic limb structures of capuchin monkeys (Aversi-Ferreira et al., 2005a, 2005b; Aversi-Ferreira et al., 2006; Aversi-Ferreira et al., 2007a, 2007b, 2007c) and others body structures were also studied (Oliveira et al., 2000; Ferreira & Prada, 2001; Silva & Ferreira, 2002; Neto & Ferreira, 2002; Silva & Ferreira, 2003; Silva et al., 2003; Lima et al., 2003).

The knowledge on the macroscopic internal structure of Cebus will provide data for histological and biochemical studies and contribute in ethological studies and the preservation of the species.

Behavior, memory, use of tools and encephalization index have put the Cebus genus near to chimpanzees in relation to these aspects. Comparative anatomic studies between Cebus and chimpanzees corroborate these data (Aversi-Ferreira et al., 2005a, 2005b; Aversi-Ferreira et al., 2006; Aversi-Ferreira et al., 2007a, 2007b, 2007c) in relation to muscles, nerves and vessels of the thoracic limbs.

Aversi-Ferreira et al. (2007a, 2007b) demonstrated that the arterial distribution of arm and shoulder of Cebus presents a standard that privileges their arborous behavior. Studies on nerves were conducted by Ribeiro (2002) on brachial plexus without comparison with others animals, and studies on the nerves of the arm (Aversi-Ferreira et al., 2005b) have demonstrated identical enervation between Cebus, humans, chimpanzee and baboons, therefore there is divergence of trajectory of the nervous of arm between these species.

These studies indicate an important association between anatomical data with behavioral aspects, mainly in relation to Cebus, because any authors indicate that Cebus can be used like models to anthropological studies how is done to Old World Monkeys (Westergaard & Fragaszy, 1987; Visalberghi et al. 1995; Tavares & Tomaz, 2002; Waga et al. 2006; Aversi-Ferreira et al., 2006). Therefore, anatomical studies on Cebus anatomy are urgent to generate basis to behavioral, physiological and ecological studies on this species; furthermore, mistakes can be made, because behavioral and ecological studies rarely consider anatomical aspects of target species.

The objective of this study is to characterize the nerve model of the forearm and hand of the Cebus monkey. For this, the main nerves and their branches located in the forearm and hand of the Cebus monkey was anatomically characterized, taking into consideration their frequency, number, origin and distribution. The data was related with the same nerves found in specialized literature for humans (Gardner et al., 1988; Spence, 1991; Testut & Latarjet, 1958), and in specialized literature for other non-human primates (Swindler & Wood, 1973).

MATERIAL AND METHOD

In this study, 7 Cebus libidinosus (Rylands et al., 2000) monkeys were used (1 female and 6 males), all healthy adults, with deviations as for size and age. The monkeys were provided by IBAMA (Brazilian Institute for the Environment and Renewable Natural Resources), from the city of Sete Lagoas, State of Minas Gerais, in 1970, and housed at the anatomy collection of the Goiás Federal University (UFG). All animals were prepared with injections of Neoprene 601A latex (DuPont) on the femoral artery. The animals were carefully dissected at naked eye or with the aid of 10x stereoscopic magnification.

 

RESULTS

The dissection and description of nerves that are distributed in the forearm of the Cebus monkey start from the elbow joint at the medial epicondyle, point where the three main nerves of the arms reach the forearm.

Generally, the radial nerve has superficial position in relation to the ulnar nerve, being located laterally in the forearm in two proximal thirds and in the distal third, its superficial branch passes through the posterior side of the forearm and reaches the back of the hand.

The ulnar nerve has deep position in relation to the radial nerve. After emerging in the forearm, in the description of its proximal-distal path, it passes through the ulnar groove humerus medial epicondyle, and in a distal position in the forearm, it crosses the carpus joint and penetrates the hand, which generates the muscular and digital branches.

The median nerve reaches the forearm after passing through the supra-epicondylar foramen of the humerus, as reported by Aversi-Ferreira et al. (2005b), along with the ulnar artery, and follows a distal path in lateral position in Cebus throughout the forearm, and in the distal portion, near the carpus, the median nerve penetrates the carpus under the flexor retinaculum, and generates muscular and digital branches in the hand.

Description and comparison of nerves (Table I)

Radial nerve. The radial nerve (Fig.1) reaches the forearm between the insertion tendons of the brachial and brachial biceps muscles and the origin tendon the brachioradial muscle below the lateral epicondyle. In the cubital fossa, it generates muscular branches for brachioradial muscle, distal portion of the brachial muscle, proximal portion of the long radial extensor muscles of the carpus and short radial extensor muscles of the carpus. In the forearm, yet in cubital fossa, the radial nerve is divided into a superficial branch and a deep branch.

Fig. 1. Photograph of the anterior view of the cubital fossa of the Cebus right forearm.

1. Radial nerve.

2. Superficial branch.

3. Deep branch.

4. Brachial muscle.

5.Brachioradial muscle.

Bar=1,2cm.

1. Superficial branch of the radial nerve. The superficial branch (Fig.2) of the radial nerve follows in the distal direction through the lateral face of the forearm, covered by the brachioradial muscle and the long radial extensor muscles of the carpus. It is followed medially through the radial artery up to the distal third of the forearm, which passes through the dorsal position in relation to the tendon of the abductor muscle long the thumb, and generates an anterior branch (ventral) and a posterior one (dorsal).

Fig. 2. Lateral view of the right forearm of the Cebus with the black arrow evidencing the superficial branch of radial nerve.
(1) Long radial extensor of the carpus muscle; (2) extensor of fingers muscle. Bar=1cm.

 

The posterior branch reaches the dorsal region of the distal third of the forearm under the brachioradial muscle and on the tendons of the long abductor muscles and short extensor muscle of the thumb; soon after, it generates branches to the medial face of the thumb, II and III fingers and to the lateral faces of II and III fingers.

The anterior branch follows up to the lateral region of the wrist joint covered by the tendon of the brachioradial muscle, long radial extensor muscle and short extensor muscle of the carpus.

In the back of the hand, the dorsal branch of the nerve generates branches to the medial and lateral faces of thumb and II, III and IV fingers. In the IV finger, the innervation sometimes occurs in the medial face.

In one case studied, the muscular branches emerged before the cubital fossa for the following muscles: brachioradial, brachial and long radial extensor of the carpus, and the branches for the fingers emerged proximally in relation to the general description.

Fig. 3. Medial view of the left forearm of the Cebus with the flexor ulnar of the carpus muscle was folded.
(1) Ulnar nerve; (2) superficial branch; (3) styloid process of the ulna. Bar=1cm.

Fig. 4. Medial view of the rigth forearm of the Cebus. (1) Median nerve; (2) anterior interosseous nerve. Bar=1cm.

2. Deep branch of the radial nerve (posterior interosseous nerve). In all animals dissected, only one deep branch of the radial nerve was found.

After passing through the lateral epicondyle of the humerus, this branch follows to the supinator muscle and generates a branch for this muscle, in one case, and in other cases, the deep branch (Fig.1) of the radial nerve crosses the supinator muscle and innervates it. In its path early in the middle third of the forearm and in accordance with the descriptions in other species of primates, the deep branch of the radial nerve is called posterior interosseous nerve, is covered by common extensor muscles of the fingers and is on the long abductor of the thumb muscle. In the distal part of forearm this nerve runs deeply and anterior to long extensor of the thumb. This nerve innervates the common extensor muscles of the fingers, long extensor of the thumb, ulnar extensor of the carpus and long abductor of the thumb.

Ulnar nerve. The ulnar nerve (Fig. 3) was found in all dissected forearms. This nerve reaches the forearm through the groove of the ulnar nerve in the medial epicondyle of the humerus under the origin tendon of the ulnar flexor muscle of the carpus, for which it generates a branch, which is found between tendons of the superficial and deep flexor muscles of the fingers, muscles that receive branches of this nerve. When passing through the elbow joint, just after the cubital fossa, the division into superficial and deep branches of the ulnar nerve is evident. At the beginning of the middle third of the forearm, the deep branch of the ulnar nerve generates a dorsal branch for the ulnar flexor muscle of the carpus and for the dorsal medial portion of the hand. Both superficial and deep branches follow separate and adjacent to one another, located at the medial face of the forearm parallel to the ulnar artery in the two distal thirds of the forearm.

In the distal third, they present superficial position and penetrate the carpus. The superficial branch passes between the tendon of the ulnar flexor muscle of the carpus and styloid process of the ulna and laterally to the psiform bone of the hand, where it distributes branches for the medial portions of IV and V fingers and lateral of the V finger. In the hand, the superficial branch of the ulnar nerve follows the ulnar artery in its path under the short palmar muscle, innervates this muscle and generates four branches: one deep branch that innervates the hipotenar muscles, contracting muscles, interosseous palmar muscles and dorsal interosseous muscles, and the other three branches form the digital nerve of V finger, the common digital nerve of IV and V fingers and a communicating branch with the median nerve that forms the common digital nerve of III and IV fingers.

The deep branch of the ulnar nerve is much thinner than the superficial branch, passes through the flexor retinaculum and medially to the psiform bone and in the hand, it generates branches for the medial and lateral faces of IV and V fingers.

Median nerve. In all dissected animals, only one median nerve (Fig. 4) was found. The path of this nerve in the forearm starts up after its emergence in the cubital fossa through the supra-epicondylar foramen of the humerus. In the cubital fossa, it generates many small branches; however, an anterior interosseous branch stands out. In 6 animals, the median nerve reached the forearm through the supra-epicondylar foramen of the humerus followed by the ulnar artery, separating from it after passing through the cubital fossa, but in one case, the nerve does not pass through the supra-epicondylar foramen.

In the proximal third of the forearm, the following sequence in its path could be verified: 1) it is initially found in the medial face of the tendons of the brachial biceps and brachial muscles, under the teres pronator muscle, 2) it moves deeply to the teres pronator muscle in six verified cases, and crosses this muscle in one of the cases, but in all cases, it generates a muscular branch for the teres pronator muscle and in this region, it is on the deep flexor muscle of the fingers, 3) after emerging under the teres pronator muscle, it is found on the deep flexor muscle of the fingers, covered by the radial flexor muscle of the carpus, laterally to the superficial flexor muscle of fingers.

It follows to the forearm at the middle third, covered by the superficial flexor muscle and on the deep flexor muscles of the fingers, which is frequently adhered to the fascia of this muscle.

It reaches the wrist, passes through the carpus channel where it is covered by the tendon of the long palmar muscle. Soon after crossing the carpus channel, it subdivides for the thenar muscles and medial face of the thumb, and medial face of II and III fingers. In some cases and in antimers of the same animal, branches for the lateral face of the IV finger were observed.

The median nerve enters the hand through the carpus tunnel, passing through the retinaculim of flexor muscles and generates five terminal branches: the most medial is the one that attaches to the communicating branch of the ulnar nerve; the digital nerve common for II and III fingers, the digital nerve of II finger, digital nerve of the thumb, the recurrent branch that innervates the thenar muscles, except for the adductor muscle of the thumb, which is also innervated by the deep branch of the ulnar nerve.

1. Anterior interosseous nerve. In all cases, no more than one anterior interosseous nerve (Fig.4) was found. In all cases, the anterior interosseous nerve emerges from the median nerve dorsally, as soon as it reaches the forearm in the cubital fossa and then passes the teres pronator muscle and generates a branch for the radial flexor muscle of the carpus.

After a short deep route, it reaches the anterior face of the interosseous membrane, following distally and being covered by the superficial flexor muscle of the fingers and followed laterally by the anterior interosseous artery up to the proximal margin of the teres pronator muscle, following toward the carpus. The nerve was not observed in the hand of these animals.

DISCUSSION

Radial nerve. Testut & Latarjet, Gardner et al. describe only one radial nerve in humans, and Swindler & Wood also describe only one radial nerve in baboons and chimpanzees. Swindler & Wood describe the radial nerve in the cubital fossa for chimpanzees, baboons and humans similar to what was described here for Cebus, which is the same given by Gardner et al. and Testut & Latarjet.

In the forearm, the radial nerve is divided into a superficial branch and a deep branch, and in chimpanzees, baboons and humans, the same aspect is observed (Swindler & Wood; Gardner et al.; Testut & Latarjet). Swindler & Wood reported that the radial nerve is divided into superficial and deep branches in the cranial portion of the cubital fossa, and deeply to the brachioradial muscle.

1. Superficial branch of the radial nerve. The same general description is made for humans for the superficial branch of the radial nerve according to Testut & Latarjet and Gardner et al.; however, Testut & Latarjet reported that in the beginning of the superficial branch path, this is adjacent to the anterior recurrent artery up to the insertion of the biceps muscle in the tuberosity of the radium, from which the relationship with the radial artery starts. Swindler & Wood describe only that this branch is in the forearm covered by the brachioradial muscle and do not mention relations with other muscles.

In the back of the hand in Cebus, this nerve generates branches for the medial and lateral faces of thumb and II, III and IV fingers. In IV finger, the innervation verified for this nerve sometimes is only found in the medial face, and the general description given here for Cebus is identical to humans (Testut & Latarjet; Swindler & Wood; Gardner et al.). In chimpanzees and baboons, according to the description of Swindler & Wood, these aspects are the same as in Cebus for the forearm, but these authors did not mention the dorsal branches of the superficial branch of the radial nerve in the hand.

2. Deep branch of the radial nerve (posterior interosseous nerve). In Cebus, after passing through the lateral epicondyle of the humerus, the posterior interosseous nerve has direct relationship with the supinator muscle and innervates it, has distal path and is called the posterior interosseous branch, which is identical in humans (Testut & Latarjet; Gardner et al.). Swindler & Wood describe the path of this nerve in the proximal portion of the forearm for chimpanzees and baboons, which crosses the supinator muscle, description similar to what occurs in Cebus, and also report that the superficial branch of the radial nerve that follows the distal path within the carpus, but the latter aspect has not been seen in Cebus.

Ulnar nerve. Testut & Latarjet called the superficial and deep flexor muscles of the fingers as satellite muscles of the ulnar nerve by following that nerve in its path through the forearm, similar in the description of Cebus. The path, innervation and location of the ulnar nerve in Cebus are identical to what occurs in humans (Testut & Latarjet; Swindler & Wood; Gardner et al.), chimpanzees and baboons (Swindler & Wood). In humans, the authors (Testut & Latarjet; Swindler & Wood; Gardner et al.) did not mention a branch of the ulnar nerve for the IV finger, as in Cebus. Besides the fact that the origins of the superficial, deep and dorsal branch of the ulnar nerve occurs in Cebus in the proximal portion of the forearm, data that do not occur normally in humans are found and no reports in relation to this aspect for chimpanzees and baboons are found.

In humans, it is not reported that the ulnar nerve innervates the deep flexor muscle of the fingers (Testut & Latarjet; Swindler & Wood; Gardner et al.), as occurs in Cebus and baboons (Swindler & Wood).

Median nerve. The median nerve passes deeply to the teres pronator muscle in six cases verified and crosses the muscle in one of the cases; the description is identical for humans (Gardner et al.), chimpanzees and baboons (Swindler & Wood). The path, innervation and location of the median nerve in Cebus is in agreement with the descriptions reported for humans (Testut & Latarjet; Swindler & Wood; Gardner et al.), chimpanzees and baboons (Swindler & Wood).

1. Anterior interosseous nerve. The description for the anterior interosseous nerve made for Cebus is identical to humans (Testut & Latarjet; Swindler & Wood; Gardner et al.), but the nerve is not described by Swindler & Wood for chimpanzees and baboons.

General Considerations, The work on muscle and nerves of Cebus (Aversi-Ferreira et al., 2005a, 2005b; Aversi-Ferreira et al., 2006; Aversi-Ferreira et al. 2007c) were unanimous in verifying that the general patterns of nerve in the thoracic limbs of these animals is similar to that of other primates (chimpanzees, baboons and humans) but the location and path are unequal, perhaps due to the existence in Cebus of structures, such as the supra-epicondylar foramen and the dorsoepitroclear muscle.

The main differences between these animals in relation to thoracic limbs are the insertions of muscles and the individuality of their belly. For the nerves of the forearm of Cebus, no variations in the nerve pattern of the muscles were observed, except for the deep flexor muscle of fingers, which in Cebus and baboons is innervated by the ulnar nerve and in humans and chimpanzees it is performed by the median nerve; however, these nerves exchange fibers with one another and in the brachial plexus, according to Gardner et al.

Innervation variations may occur in the fingers of Cebus in relation to other primates, but these variations are reported with variation in humans.

This identical innervation pattern in relation to the nerves of the arm (Aversi-Ferreira et al., 2005b), forearm and hand in Cebus and others Old World primates and humans is one important justify the use of this monkey as model for anthropological evolutionary studies (Aversi-Ferreira et al., 2005b).

CONCLUSION

In general, the innervation pattern in the forearm of Cebus is identical to that of other primates studied (chimpanzees, baboons and humans), except for the innervation through the ulnar nerve of the deep flexor muscle of fingers in Cebus and baboons.

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Correspondence to:

Dr. Tales Alexandre Aversi-Ferreira.

Integrated Biochemistry and Neurosciences Laboratories (LABINE) - Nursing Practices

Department of Nursery, Goias Federal University,

Campus of Catalão.

Avenida Dr. Lamartine Pinto de Avelar N 1120,

Setor Universitário, 75404-020, Catalão-GO

BRASIL

Email: aversiferreira@gmail.com

Received: 17-12-2008

Accepted: 04-02-2009

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