Comparative Anatomy of the Peripheral Nerves

Chapter 5

Comparative Anatomy of the Peripheral Nerves Malcon Andrei Martinez-Pereira1,2,* and Denise Maria Zancan2 1

Health Sciences Center, University of Cruz Alta, Cruz Alta, Rio Grande do Sul, Brazil. 2 Neurobiology Laboratory, Physiology Department, Institute of

Basic Health Sciences, Federal University of Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil. *Corresponding author: e-mail: [email protected]

The peripheral nerves comprise the cranial and spinal nerves linking the central nervous system to the peripheral tissues. The numerous axons are sheathed individually by Schwann cells (myelinated axons) or in multiple manner (unmyelinated axons) and carry specific afferent or efferent information. Each one of these nerve fibers has anatomic and physiologic properties to achieve their functional roles. These nerve fiber axons display different arrangements as they course throughout the peripheral nerves. The nerves, in turn, may be organized in networks of entanglements and anastomosis of various branches of nerves, which constitute the neural plexuses. Sets of spinal nerves that serve the same body area are arranged into one large group of nerves. Enlargements called intumescences are found in the spinal cord. They are characterized by an increase in the number of cells and nerve fibers and located in the cervical and lumbar regions. These intumescences correspond to the formation of the brachial and lumbosacral plexuses that will innervate the thoracic (forelimb) and pelvic limbs (hindlimb), respectively. A knowledge of the origin, route, and destination of the plexus components is important to clinical practice and surgery. The mapping provided can correlate each nerve to the innervated end organ, allowing a precise investigation of the neurological damage. Peripheral nerve lesions are very common in the routine of emergency care in hospitals. This information is also necessary during treatment of, or for rehabilitation from, various diseases in which it is necessary to use intravenous or intramuscular medications and perform locoregional anesthesia and surgical interventions, decreasing the risk of iatrogenic injury and aiding in the examination and diagnosis of injuries. Thus, we see the importance of knowing the plexuses, but also the variations of nerve origin and distribution. This chapter provides a comparative review of the topography, origin, and distribution of the nerves that constitute the brachial and lumbosacral plexuses. Anatomical descriptions are presented comparing the spinal cord and plexus of Nerves and Nerve Injuries, Vol. 1. http://dx.doi.org/10.1016/B978-0-12-410390-0.00005-6 © 2015 Elsevier Ltd. All rights reserved.

humans and mammal species recognized as experimental models in the study of plexopathies and peripheral nerve injuries, such as the rat (Rattus norvegicus), the guinea pig (Cavia porcellus), the chinchilla (Chinchilla lanigera), the rabbit (Oryctolagus cuniculus), dogs, cats, swine, and nonhuman primates. To understand a little better the features of design that characterize a mammal organism, we must interpret its structure from a comparative perspective, including the lower tetrapods in the analysis of brachial and lumbosacral plexuses, even though there are fewer available reports on amphibians and reptiles, or even birds, than on mammals. Descriptive morphology is important for the analysis of animal design, and the considerable variation in the anatomy of the tetrapod brachial and lumbosacral plexuses is due to the remarkable variation in limb shapes and modes of locomotion.

SPINAL CORD AND SPINAL NERVES The number of spinal cord segments in each region (cervical, thoracic, lumbar, sacral, and coccygeal) is variable between species and is presented in Table 5.1. The diameter of the spinal cord is not uniform, due to enlargements in the cervical and lumbar regions, characterized by an increase of cells and nerve fibers, which was referred to earlier in this chapter. Cranially, the spinal cord is limited to the medulla oblongata at the level of the foramen magnum of the occipital bone. This border is not well defined and is often rostral to the origin of the first cervical nerve. The end of the spinal cord is tapered to form the conus medullaris, which continues with a thin meningeal filament, the filum terminale. The topography of the conus medullaris varies according to the species and age of the animal, occurring between the last lumbar vertebra (basis) and first sacral one (apex). This knowledge is important to support clinical and surgical procedures such as spinal puncture, to locate the central nervous lesions at specific vertebral levels, 55

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Cervical Region

Thoracic Region

Lumbar Region

Sacral Region

Coccygeal Region

Species

Vertebrae

Spine Segments

Vertebrae

Spine Segments

Vertebrae

Spine Segments

Vertebrae

Spine Segments

Vertebrae

Spine Segments

Human

7

8

12

12

5

5

5

5

1

1

Nonhuman Primates Ateles

7

8

14

14

4

4

3

3

25

5

Cebus

7

8

14

14

5-6

5-6

3

5

23

4

Chimpanzee

7

8

13

13

4

4

6

6

1-2

1

Cynomolgus

7

8

12

12

6-7

6-7

3-4

3-4

25

7

Gibbon

7

8

13

13

5

5

5

5

1

1

Gorilla

7

8

13

13

4

4

5

5

1-2

1

Lagothrix

7

8

14

14

4

4

3

3

25-27

5

Orangutan

7

8

12

12

4

4

5

5

1

1

Rhesus

7

8

12

12

6-7

6-7

3-4

3-4

25

7

Cat

7

8

13

13

6

7

3

3

20-23

5

Chinchilla

7

8

12

12

6

6

4

4

20-23

4

Dog

7

8

13

13

7

7

3

3

20-23

5

Guinea pig

7

8

13

13

6

6

4

4

1-3

3

Swine

7

8

14-15

15

6-7

6

4

4

20-23

5

Rabbit

7

8

12

12

7

7

4

4

5

3

Rat

7

8

12-13

12-13

6

6

4

4

20-23

3

Other Mammals

PART I History, Histology and Development of the Peripheral Nerves

TABLE 5.1 Number of Vertebrae and Medullar Segments per Region of the Spinal Cord in Different Species

Comparative Anatomy of the Peripheral Nerves Chapter 5

and to identify the most suitable point for the application of epidural anesthesia without damage, because it depends on the location of the spinal cord end in distinct animal species. Comparative topography of the conus medullaris in different species is summarized in Table 5.2. The cauda equina is located caudally to the conus medullaris. It consists of nerve roots located inside the spinal canal of the lumbar and sacral spine, together with the medullar cone and terminal filament, with variable location in the animals. An injury in this region might involve several nerves, because the cauda equina contains a large number of nerve roots in a small area located between L3 and S3.

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The cauda equina includes the main nerves of the lumbosacral plexus. The histological structure of the gray matter of the spinal cord is the same in all mammalian species. The dorsal horn constitutes the afferent integration center, whereas the ventral horn contains the motor neurons innervating the skeletal muscles. An intermediate zone of gray matter consists of intermediolateral nuclei of the autonomic nervous system. The cell bodies are organized in laminae arranged dorsoventrally in the gray matter (Figure 5.1). Laminae I to VI in the dorsal horn, laminae VII and VIII in the intermediate zone, the motor neuron groups constitute lamina IX,

TABLE 5.2 Level of Cervical and Lumbar Intumescences and Conus Medullaris of Spinal Cords in Some Vertebrates Species

Cervical Intumescentia

Lumbar Intumescentia

Conus Medullaris

Human

C4-Th1

Th11-L1

L1-3

Ateles

C4-Th2

L1-4

L5-S2

Cebus

C4-Th2

L1-4

L5-S3

Chimpanzee

C4-Th1

Th11-L1

L1-3

Cynomolgus

C4-Th2

L1-4

L5-S3

Gibbon

C4-Th1

L1-4

L3-S3

Gorilla

C4-Th1

Th11-L1

L1-3

Lagothrix

C4-Th1

L1-4

L1-S2

Orangutan

C4-Th1

Th11-L1

L1-3

Rhesus macaque

C4-Th2

L1-4

L1-S3

Cat

C3-Th1

L3-5

L5-S3

Chinchilla

C5-Th2

L2-L5

L6-S2

Nonhuman Primates

Other Mammals

Dog

C4-Th1

L4-6

L3-7

Guinea pig

C4-Th1

Th12-L2

L5-S2

Swine

C4-Th1

L6-7

L5-S3

Rabbit

C5-Th2

Th12-L2

L5-S4

Rat

C5-Th1

Th11-L1

L1-3

Birds

C11-Th2

Synsacrum

Synsacrum

Crocodilians

SN6-11

No information

No information

Iguana

C8-PS3

PS25-28

PS28-S2

Varanus

C9-PS2

PS28-30

PS30-S2

Tortoise

C5-Th1

Th6-S1-5-Co1

No information

Anurans

SN1-3

SN7-10

S1-Urostyle

Other Tetrapods

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PART I History, Histology and Development of the Peripheral Nerves

FIGURE 5.1 Summary of the laminar organization of the spinal gray matter. In the dorsal horn are located the projections of sensory neurons (laminae I to VI), which are found in the ganglia of the spinal nerves. In the dorsal horn there are also interneurons that communicate the projections of afferent neurons, which reach the spinal dorsal spine, with the efferent or motor neurons. The cell bodies located in the ventral horn originate axons that form bunches of fibers that will innervate muscles and viscera, and are called efferent or motor neurons or inferior motor neurons (laminae IX and X). Laminae VII and VIII correspond to the lateral horn or intermediate zone. Within the lateral horn are located the intermediomedial and intermediolateral nuclei of the autonomic nervous system in the thoracic and high lumbar segments of the spine cord. Created by Vagner Geschwind Basso (2013).

and lamina X corresponds to the gray matter surrounding the central canal. The peripheral nervous system (PNS) consists of cranial and spinal nerves, including their roots, and distal branches with receptor endings and ganglia. The architecture of a peripheral nerve was described in Chapter 4. Three types of nerve fibers constitute the peripheral nerves: sensory, motor, and autonomic, and each nerve bundle may contain both afferent and efferent fibers of various types. As mentioned, primary afferent or sensory fibers collect information through receptors in the periphery of the body (skin, muscles, and tendons) or wall of the viscera, entering the spinal cord through the dorsal roots of the spinal nerves. The afferent fibers of peripheral nerves, myelinated or unmyelinated, may be classified according to their diameters as described in a previous chapter. The Aδ and afferent fibers terminate in lamina II. All these fibers are connected to interneurons located at the border of laminae V, VI, and VII and/or to interneurons in laminae I, II, and III, both of them terminate in ipsi- and contralateral motor neuron groups. The efferent fibers are alpha (70-120 m/s) and gamma (15-30 m/s) fibers. Alpha fibers are responsible for generating muscle force and form the motor unit with

the muscle fibers they innervate, whereas gamma fibers innervate the intrafusal muscle fibers located at the poles of the muscle fibers and inform the variations in the length of the muscle. The other efferent fibers are the preganglionic autonomic fibers (group B; 3-14 m/s), which are small-sized (
3 μm) and moderately myelinated. The origin of the spinal nerve reveals the segmentation of the spinal cord. The number of spinal nerves varies according to the animal species and the number of vertebrae or spinal cord segments, with the exception of the cervical cord, which is constant in almost all species. The first pair of spinal nerves emerges from the spinal cord between the base of the skull and the first cervical vertebra. The remaining cervical nerves are situated cranially to their corresponding vertebrae, with the exception of the eighth pair of cervical nerves, which emerge cranially at the first thoracic vertebra. From Th1, all spinal nerves emerge below their corresponding vertebrae, even those that constitute the cauda equina. The number of spinal nerves in each spinal region and the total of the nerves in each species that correspond to spinal segments are shown in Table 5.1. The neuroanatomy and cytoarchitecture of the encephalic structures, particularly the cerebral cortex (pallial domains),

Comparative Anatomy of the Peripheral Nerves Chapter 5

of avian and mammalian species are much varied. In contrast, the PNS is very similar in several cytoarchitecture features and anatomical arrangement. The spinal nerves in birds are called cervical, thoracic, lumbar, sacral, and coccygeal nerves, whose number usually corresponds to the number of vertebrae of each region and therefore varies across bird species. The best method to determine the spinal nerves is by counting the number of vertebrae, starting at the base of the skull caudally.

BRACHIAL PLEXUS The brachial plexus is a somatic nerve plexus formed by intercommunications among the ventral rami (roots) of the inferior cervical nerves and the first thoracic nerves. The plexus is responsible for the sensory and motor innervations of the scapular, pectoral, and thoracodorsal regions and the thoracic limb. After the formation of the spinal nerve, there occurs a serial anastomosis that originates three common trunks ((C4-5)C6; C7-8, C8-Th1(Th2)) culminating in the formation of divisions, cords, and branches. There are five “terminal” branches and numerous other “preterminal” or “collateral” branches that leave the plexus at various points along its length. The brachial plexus communicates with the sympathetic trunk via gray ramus communicans, which join the roots of the plexus. They derive from the middle and inferior cervical sympathetic ganglia and the first thoracic sympathetic ganglion. Knowledge of applied anatomy is crucial for a good neurological examination in a brachial plexus injury, particularly in situations where the imaging facilities are poor. It is necessary to emphasize applied clinical anatomy skills during undergraduate and postgraduate training of medical students and surgery residents. The brachial plexus is a particularly critical portion of the PNS due to its special anatomical relationships with mobile structures of the neck and shoulder, which may be involved when the force vectors cause traction on these structures resulting in trauma. Additionally, the relative lack of protective muscle and bone can result in penetrating injuries of the region. The brachial plexus injuries usually affect the dominant thoracic limb, but there are situations where both limbs are affected. The pathophysiological mechanisms of traumatic injury include traction, avulsion, crush, partial or total rupture of the nerve roots, and injury accompanied by posttraumatic edema secondary to trauma. Cases of complete brachial plexus injury present a poor prognosis with almost no possibility of recovery.

Human Brachial Plexus The human brachial plexus is described in this chapter to allow a comparison with other primates, described below. The brachial plexus is formed by spinal nerves or roots of

59

C5-8 and Th1. When the root of C4 externally contributes to the brachial plexus, this formation is called prefixed, while the contribution of Th2 is called postfixed. The roots form three trunks: superior or cephalic (C5-6), medium (C7), and inferior or caudal (C8-Th1). In short, the roots of C5-C6 (axillary and musculocutaneous nerves) are responsible for the movements of the shoulder and elbow flexion, while the C6-8 (radial nerve) is responsible for controlling the extensor muscle group of the elbow, wrist, and extrinsic thumb and fingers. The long thoracic (C5-7), suprascapular (C5-6), dorsal scapular (C4-5), short supinator (C6), and subclavian (C5-6) nerves have an important stabilizing function of the shoulder. The roots of C6-8 and Th1 (median nerve) and C8-Th1 (ulnar nerve) provide motor innervation to much of the extrinsic flexor muscles group and intrinsic muscles, being responsible for the motricity and the grasping ability of the hand. Distally, the brachial plexus gives rise to other branches with direct anatomical expression: the thoracodorsal (C7), the superior and inferior subscapular (C7), and the lateral (C5-6) and medial (C8-Th1) pectoral nerves.

Nonhuman Primates There has been great interest in the study of nonhuman primates because of the anatomical, physiological, and ethological similarities of these animals with humans. These similarities are important from the evolutionary perspective to understand human development. The description of the brachial plexus in this section is based on three genera of Hominidae (Gorilla, Pan or chimpanzee, and Pongo or orangutan), on the genus Hylobates (gibbon; superfamily Hominoidea), and some primate species of experimental interest such as Cebus apella, Macaca mulatta, Lagothrix lagothricha, and Ateles. Data on the functions of the distribution of segmental nerves in the rhesus macaque (Macaca mulatta) were particularly important because they provided major information on the functions of the spinal reflexes. These experiments allowed us to establish accurate maps of cutaneous individual and adjacent territories of innervation, currently being used to understand human neurophysiology. What seems most striking when comparing the plexuses of man and other primates, mostly the rhesus macaque, is not the slight difference in organization described most frequently, but the many points of striking similarity into the basic plane. Plexus branches, in supraclavicular and infraclavicular divisions, are very similar to those observed in man, especially when the individual distribution of each nerve is considered. In their pathway from the neck to the axillary region, the brachial plexus elements in nonhuman primates are subject to the various types of mechanical injuries that occur in humans. This becomes clear when one bears in mind that the nervous structures, from their intraforaminal components to

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PART I History, Histology and Development of the Peripheral Nerves

the formation of the various nerves in the periphery, cross numerous osteoligamentous and aponeurotic features that exist in the wide-area mobility and fulcrum of movements, such as the cervicobrachial segment. Structural studies suggest that the inferior roots are more susceptible to avulsion than the superior roots, which suffer further damage by stretching or rupture in continuity after the vertebral foramen. Nevertheless, injury of the superior trunk is believed to be the most frequent lesion of the brachial plexus, representing one-third of all plexus injuries. In arboreal primates, such as Cebus and Lagothrix, brachial plexus injuries can result from abrupt downward force (adduction) against the shoulder and the head is forced concurrently to the opposite side. In this situation, the superior portion of the brachial plexus is more committed. However, a sudden upward traction of the upper limb, associated with abduction and internal rotation, results in lesions of inferior cervical roots. The condition of avulsion of inferior cervical roots has a better prognosis. The brachial plexus is formed by C5 to C8 and Th1 spinal nerves in gorillas, chimpanzees, orangutans, gibbons, rhesus macaque, Cebus, Lagothrix, and Ateles. However, the facultative presence of C4 is a constant in these animals. In the prefixed plexuses of Hominoidea there is another contribution of C4, which is not observed in other primate groups. Furthermore, an extreme degree of prefixation of the plexus is found in gorillas where C5-6 are very long and Th1 is very short, as is observed in humans. Thus, considering the increase of the number of branches in the formation of the brachial plexus, one might suppose that the inclusion of C4 in the higher primates indicates an evolutionary trait of the brachial plexuses in Hominidae. Like in humans, the primate spinal nerves, after emerging from the intervertebral foramen, constitute three common trunks: cephalic or superior or cranial (C5-6), medium (C7), and caudal or inferior (C8-Th1) (Figure 5.2). However, in the rhesus monkey the presence of a root trunk is described, which provides the following organization: trunk circumference (C5-6), intermediate cranial (C6-7), intermediate flow rate (C7-8), and caudal (C8-Th1). In nonhuman primates the nerves are organized according to the trunk of origin (superior, medium, and inferior trunks) or to its functional character (extensor and flexor groups), and likewise in humans. In the extensor group, nerves predominate originating from the dorsal and medium trunks (dorsal scapular, long thoracic, suprascapular, subscapular, thoracodorsal, axillary, and the branch of the teres major muscle and radial). The dorsal scapular nerve arises at C4 (gorilla and chimpanzee), C5 (gibbon and orangutan), and contributions of C5 to C4 in prefixed plexuses of the Cebus, Ateles, and rhesus macaque. In Cebus, gorillas, and orangutans the long thoracic nerve arises from C5-6, in chimpanzees it emerges from C6-8, and in gibbons and the rhesus macaque it originates from

C6-7, whereas in Ateles it arises from C5-7. In the prefixed plexus of chimpanzees and gorillas, the suprascapular nerve originates from C4-6, but in other primates it originates from C5-6. The exception is the gibbon where it arises only from C5. The number of subscapular nerves ranges from three to five groups in the primates and is derived from C5-6 in the rhesus macaque, Lagothrix, and Ateles, and from C5-7 in gorillas, C7-8 in Cebus, and C8-Th1 in orangutans and chimpanzees. The thoracodorsal nerve is only described as it arises from C7 in the gibbon, but in other species it emerges from C6-8 in Cebus, C7-8 in the rhesus macaque, and C8 and Th1 in Lagothrix. The axillary nerve of the Hominidae primate is described as having a similar origin as observed in humans (C5-6), but in Ateles, Cebus, and rhesus macaque it emerges from C5-8 and a broader origin (C5-8) is described in Lagothrix. The branch to the teres major muscle is described as derived from the axillary nerve in rhesus macaque and Ateles; however, this is described as an independent nerve from the C7 in Cebus and from C6-7 in chimpanzees. A wide range of combinations is seen at the origin of the radial nerve, which may arise from C5-6 in Ateles, C5-8 in hominids and Cebus, and from all trunks (C5 to Th1) in Lagothrix. The flexor group consists of nerves originating from the dorsal trunk (anterior thoracic, subclavian and musculocutaneous) and midventral (median, ulnar and brachial, and antebrachial medial cutaneous nerves). However, some nerves, despite belonging to a functional group or being derived from the same trunk, can provide a differentiated formation between the primate species. Similar to humans, the medial (medial pectoral nerve) and lateral (lateral pectoral nerve) thoracic nerves originating from C5-6 and C8Th1, respectively, are observed in apes. However, in the rhesus macaque, when the lateral nerve has two nerve roots, one originates from C7 and another from C8-Th1, and the medial nerve arises from C5-6. In contrast, in Cebus and Lagothrix, the medial nerve arises only from C8, but the lateral nerve emerges from C7-8 in Cebus and only from C7 in Lagothrix. The subclavian nerve can originate jointly from the phrenic nerve (C5-6) in Cebus or as an independent branch of this trunk in the gorilla, chimpanzee, and rhesus or even only from C6 in gibbons and Ateles, being absent in orangutans. In all nonhuman primates described, the musculocutaneous nerve arises from the confluence of the cranial trunk (C5-6) with the medium trunk (C7), and there may be a small contribution of C4 in prefixed plexuses. The origin of the median nerve is displaced cranially to that observed in nonprimate mammals, being indicative of evolutionary changes in the composition of the plexus. Thus, this nerve originates from C8 and Th1 in Hominoidea and in the postfixed plexus of rhesus and Ateles; it has the participation of Th2, yet in the postfixed plexus of rhesus macaque their formation starts in C5. In Cebus, the median nerve originates from the confluence

Comparative Anatomy of the Peripheral Nerves Chapter 5

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FIGURE 5.2 Ventral view of the brachial plexus of Lagothrix lagothricha. (a) C4 to C7: fourth to seventh cervical vertebrae; T1: first thoracic vertebra and caudal trunk («). (b) C5 to C8: fifth to eighth cervical spinal nerves; T1: first thoracic spinal nerve and cranial ( ), medium (♦) and caudal trunks («). (c) Axillary-brachial region transition. (d) Brachial region. Musculocutaneous nerve (NMC); suprascapularis nerve (NSP); thoracodorsalis nerve (NTD); median nerve (NM); branches of the median nerve (MRI) and MRI connection with NMC (NMC + NM) with pathway to the brachial biceps muscle (5). Axillary artery (*); 1 subscapularis muscle; 3 latissimus dorsi muscle; 4 vagus-sympathetic trunk; (4-5) biceps brachialis muscle; 6 coracobrachialis muscle; 7 brachial region; 8-9 triceps brachialis muscle. Reproduced, with permission, from Cruz and Adami, 2010.

of C6 to the medium (C7) and caudal (C8-Th1) trunks forming a common nerve with the ulnar nerve at the elbow, whereas in Lagothrix it emerges from the medium trunk with a contribution from C8. Already the ulnar nerve has its origin in the caudal trunk (C8-Th1) in all primates described in this section. The antebrachial cutaneous medial nerve is the largest cutaneous nerve in primates,

because the brachial cutaneous medial nerve is an independent nerve only in Lagothrix, emerging from C8 as a common nerve for both cutaneous nerves. In Hominoidea and in Cebus the antebrachial cutaneous nerve is formed by the caudal trunk (C8-Th1), whereas in the postfixed plexus of rhesus the nerve is originated by the union between the medium and caudal trunks.

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PART I History, Histology and Development of the Peripheral Nerves

Other Mammals Experimental models for the study of brachial plexus injuries are a useful tool to understand the plexopathies. There are indeed a number of descriptions indicating some differences in the formation of the brachial plexus in different species. The different formation, position, and distribution of the structures in the brachial plexus is thought to be associated with muscle-nerve cooperation to achieve the movement, especially in muscles directed to the shoulder, thorax, and limb flexion movement. Considering that the most developed and functionally complicated brachial plexus design, related to muscle-motion coordination, is the plexus of primates, a comparative study with primates is the ideal experimental approach to obtain knowledge about brachial plexopathies. However, the most widely used experimental models are the rat, guinea pig, dog, cat, and pig, which present significant anatomical differences in relation to humans. Among these should be cited: (i) anatomical quadrupedal posture or position; (ii) absence of scapular girdle bone, by excluding the clavicle, in some species, and fusion of the coracoid to the spine of the scapula; (iii) modification of attachment of the thoracic limb to the thorax by a synsarcosis of muscles and not by a conventional joint; and (iv) modification or loss of muscle or muscle groups. On the other hand, the distance between the nerve and its target organs is shorter in these animals, which makes it easier to observe the pathophysiology of injury and reduces the neural recovery time, allowing the assessment of the recuperation of gait and other movements with the affected limb. Peculiar characteristics, particularly the quadrupedal position, must be taken into account in choosing the animal. Thus, the researcher needs to apply the correct anatomical terms in a study with experimental animals. Most of the anatomical structures of animals are called the same as in humans, but some names change because of the standing position of the animals. Figure 5.3 illustrates a brief review of the orientation planes and axes in most vertebrate quadrupeds, as well as the terms for position, situation, and location. Didactically, when observing the animal in its anatomical position, it can be imagined within a parallelepiped. Each of the faces of the parallelepiped will be a delimitation plane. The adjacent face to the head provides the cranial plane, while the face tangent to the tail is the caudal plane; the base of the parallelepiped corresponds to the ventral plane and its opposite face to the dorsal plane; the remaining sides delimit the right and left planes. By demarcating the midpoint of two opposite planes and tracing a straight line three axes can be obtained: the craniocaudal axis, the dorsoventral axis and the latero-lateral axis. The section planes of the body are (i) the craniocaudal axis, which divides the body into right and left antimers by the longitudinal median plane; (ii) the sagittal or paramedian

planes, which are parallel to the longitudinal plane; (iii) the transversal planes, which are vertical sections on the craniocaudal axis; and (iv) the horizontal plane, which is parallel to the dorsoventral axis and divides the body into dorsal and ventral halves. For the limbs, the transversal plane divides them in proximal and distal parts in relation to the trunk. These planes and axes guide the application of the following terms to localize structures: (i) cranial and caudal (structures nearest or toward the head or tail, respectively; head structures can be also referred to as oral); (ii) dorsal and ventral (referring to backside and belly side, respectively; dorsal is also used for limb parts after the carpus and tarsus); (iii) medial and lateral (close or distant to the median plane, respectively) and intermediate (between lateral and medial structures); and (iv) palmar and plantar (posterior face of the limbs after the carpus and tarsus). The brachial plexus of vertebrate animals is formed by the contributions of the ventral rami of C6-8, Th1-2. The participation of C4 in the formation of the brachial plexus in domestic mammals, such as dogs and cats, is not described, but its involvement is observed in other species, such as rats, gorillas, and chimpanzees. According to an evolutionary hypothesis, the origin of the brachial plexus ascended in the cranial direction, reaching the fourth cervical cord in monkeys and the third cervical cord in humans. Nevertheless, the presence of C4 in the formation of the brachial plexus in marsupials and monotremes shows that the involvement of most cranial branches is not exclusive to more evolved species. The similarity of the organization of brachial plexuses in rats and humans leads to a preference for rats for experimental surgery and microsurgery studies. The brachial plexus in rats is formed by the contribution of ventral primary branches of the distal four cervical (C5, C6, C7, C8) and first thoracic (Th1) spinal nerves (Figure 5.4). The contribution of nerve fibers from C4 may be seen in rats; however, fibers from Th2 do not contribute to the brachial plexus in rats. The rabbit brachial plexus is formed by the ventral rami of (C5)C6-8, Th1(Th2), while in guinea pigs and mice the plexus originates from the ventral rami of C5-8, Th1-2, but the contribution from Th2 is controversial. The brachial plexus of the chinchilla is formed by the contributions of ventral rami of (C5)C6-8, Th1(Th2). In the dog and cat the plexus is formed by C6-8 and Th1 (C5 and Th2 may contribute significantly in some individuals), but the involvement of C5 in cats is not described and Th2, when present, is a thin branch, whereas in the pig the plexus is constituted by C5-8 and Th1, also being utilized in experimental surgery and microsurgery studies because of its similarity with the human brachial plexus. In rats it was observed that the united C5 and C6 formed the cranial (superior) trunk, C7 alone formed the medium trunk, and C8 and Th1 united to form the caudal (inferior)

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Ven tral

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ial

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tral Ros

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FIGURE 5.3 Direction planes of the animal body. The dotted areas represent the carpus and tarsus in the thoracic and pelvic limbs, respectively. Reproduced, with permission, from Dyce, Sack, and Wensing (2009). Textbook of veterinary anatomy. 4th ed. Elsevier, 2009.

trunk. However, in some cases it was encountered that C7 and C8 formed an intermediate trunk, or C7, C8, and Th1 united and formed the caudointermedium trunk instead of separate medium and caudal trunks. The brachial plexus of rabbits (Figure 5.5), guinea pigs, and mice consists of cranial (C5-7) and caudal (C8-Th1) trunks, whereas in the chinchilla it is formed by cranial (C6), medium (C7), and caudal (C8-Th1) trunks. In the dog (Figure 5.6) and cat four trunks are observed: a cranial ((C5)C6-7), intermedium cranial (C6-8), intermedium caudal (C7-8), and caudal (C8-Th1 (Th2)), while in the pig C5-6 forms a cranial trunk, C7 constitutes a medium trunk, and C8-Th1 the caudal trunk. In all these species the brachial plexus roots emerge between the cervical longus muscle and anterior and middle scalene muscles, forming a flattened plexus below the medial face of the scapula before segregating in various

combinations to form the named nerves of the thoracic limb. The brachial plexus of the described species is significantly different from the human one in several ways, namely not being easily divisible into lateral, medial, and posterior fasciculi, and frequently having a different origin of its terminal and collateral branches. The proximal nerves and territories of the brachial plexus are described hereafter. The suprascapular nerve originates from C6 in the chinchilla and cats; from C5 and C6 in the rat, rabbit, and guinea pig; and from C6-7 in the dog and pig. It crosses through the scapular incisure and innervates the proximal limb muscles (the supraspinatus, infraspinatus, and acromial part of the deltoideus muscle, when present) being accompanied by scapular vessels in its pathway. In the cat, the suprascapular nerve can send nerve branches to the subscapularis nerve. In the same region, but on the

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PART I History, Histology and Development of the Peripheral Nerves

FIGURE 5.4 Common disposition of the constituents of the brachial plexus (BP) in the Wistar rat. (a) Ventral aspect of a right forepaw dissection showing several terminal and collateral branches of the BP and their close association with the major arterial trunks (4  magnification). (b) Schematic drawing of the most common disposition of the constituents of the BP. (c) Ventral aspect of a left forepaw dissection showing the usual anastomosis between the second intercostal nerve and the medial brachial and antebrachial cutaneous nerves (10 magnification). 1 axillary nerve, 2 musculocutaneous nerve, 3 radial nerve, 4 median nerve, 5 ulnar nerve, 6 medial brachial cutaneous nerve, 7 medial antebrachial cutaneous nerve, 8 dorsal scapular nerve, 9 suprascapular nerve, 10 nerve to subclavius muscle, 11 superior subscapular nerve, 12 inferior subscapular nerve, 13 thoracodorsal nerve, 14 long thoracic nerve, 15 lateral pectoral nerve, 16 medial pectoral nerve, 17 intercostobrachial nerve, 18 axillary artery, 19 brachial artery, 20 acromial arterial trunk. Reproduced, with permission, from Ange´lica-Almeida et al., 2013.

FIGURE 5.5 Medial view of the brachial plexus in the New Zealand White rabbit. C5 caudal branch of ramus ventralis of C5, C6 ramus ventralis of C6, C7 ramus ventralis of C7, C8 ramus ventralis of C8, T1 ramus ventralis of T1, T2 cranial branch of ramus ventralis of T2. 1 suprascapularis nerve, 2 subscapularis nerve, 3 axillary nerve, 4 thoracodorsalis nerve, 5 musculocutaneous nerve, 6 radial nerve, 7 median nerve, 8 ulnar nerve, 9 lateral thoracic nerve; a subscapularis muscle, b latissimus dorsi muscle, d pectoralis ascendens muscle, e pectoralis descendens muscle. Reproduced, with permission, from Mohiuddin, Alim, Kabir, and Kashem (2011).

medial face, is the subscapular nerve formed by the ventral rami of C5-6 in the rabbit and by C5-7 in the rat, guinea pig, chinchilla, pig, dog, and cat. There are three related nerves with the lateral thorax wall: (i) the thoracodorsal nerve, which originates from C6-7 in the rat and guinea pig, from C7 in the rabbit and cat, from C7-8 in the pig, and from C8 in the chinchilla and dog (it follows thoracodorsally parallel to the blood vessel and is directed to the latissimus dorsi muscle); (ii) the lateral thoracic nerve arises from C6-8 and Th1 in the rat, mouse, and guinea pig, while in the cat, pig, and chinchilla it emerges from C8 and Th1 and from C8 and Th1-2 in the dog (it sends branches called intercostobrachial that account for the cutaneous sensitivity of the ventral thoracic and abdominal wall and the motility of the cutaneous muscle of the trunk); and (iii) the thoracic long nerve arises from C6-8 in the rat, from C7 in the cat, from C7-8 in the dog, pig and chinchilla, and from C7-8 and Th1 in laboratory rodents (it runs superficially and supplies the ventral serratus muscle). There is agreement on the existence of cranial and caudal pectoral nerves. In rats the cranial nerve arises from C5 and C6 and the caudal nerve from C7, while

Comparative Anatomy of the Peripheral Nerves Chapter 5

C6

C8 T1 9

9⬘

2 1 9⬘⬘ 6 7

3 4

7⬘

9⬘⬘⬘

4⬘ 5 8⬘

4⬘⬘ 4⬘⬘⬘ 7⬘⬘ 7⬘⬘⬘

8

FIGURE 5.6 Nerves of the right thoracic limb of the dog (medial view). 1 suprascapular nerve, 2 subscapular nerve, 3 pectoral cranial nerve, 4 musculocutaneous nerve (40 and 400 proximal and distal muscular branch, respectively, 4000 cutaneous medial antebrachial nerve), 5 medianus nerve, 6 axillary nerve, 7 radial nerve (70 triceps brachial branches, 700 branches of the extensor muscles, 7000 cutaneous cranial antebrachial nerve), 8 ulnar nerve, 80 cutaneous caudal antebrachial nerve, 9 thoracic long nerve, 90 thoracodorsal nerve, 900 lateral thoracic nerve, 9000 pectoral caudal nerve. Reproduced, with permission, from Dyce et al. (2009). Textbook of veterinary anatomy. 4th ed. Elsevier, 2009.

in the chinchilla the cranial nerve emerges from C7 only or from C7-8-Th1(2) and the caudal from C8-Th1(2), and in rabbits both nerves emerge from the caudal trunk (C7-8Th1-2). In the dog, in turn, all plexus segments (C6-8Th1) participate in the formation of the pectoral nerves, but in the cat the nerves arise from C7-8-Th1 and in the pig both nerves emerge from C7-8. The cranial pectoral nerve innervates the descending pectoral and transverse

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pectoral muscles, while the caudal pectoral nerve disperses into the cutaneous trunci and ascending pectoral muscles. The terminal and collateral nerves of the brachial plexus and their territories are described hereafter. The axillary nerve originates from C5-7 in the pig, from C7-8 in the guinea pig and dog, and from C6-7 in the rat, chinchilla, and cat, but in the rat this nerve is also described emerging from C5-8 and Th1. This nerve supplies the muscles of the shoulder joint (teres major muscle, scapular part of the deltoid muscle, and caudal portion of the subscapularis muscle) and the cleidobrachialis of the brachiocephalic muscle. The axillary nerve also sends branches that innervate the fascia and skin of the antebrachial region. The radial nerve originates from C6-8 in rats, and from C7-8 and Th1 in the rabbit, chinchilla, cat, pig, and dog with postfixed plexus. The radial nerve crosses the medial to lateral face of the antebrachial region and innervates the following muscles: anconeus, triceps brachial, brachial, tensor of the antebrachial fascia, carpus and digit extensors, long and short supinators and the skin in the craniolateral face, antebrachi, and dorsolateral face of the digit. A common trunk originating from C7-8 and Th1 forms the median and ulnar nerves, and in some species the musculocutaneous nerve. The median nerve always originates from three different roots, representing by far the thickest terminal branch of the brachial plexus of all species described. At the humerus joint, the median-ulnar common trunk disappears and the median nerve follows cranially to the olecranon to innervate the flexor carpi radialis, pronator teres, and flexor of digits 3 and 4. In addition, the median nerve supplies the skin of the medial and palmar face of the digits. At the origin the ulnar nerve is superficial and reaches to the olecranon, changes its course and innervates the carpal joint flexor (flexor carpi ulnaris and interosseous) and digit (profound digital flexor) muscles, the caudal cutaneous antebrachial branch, and the skin of the lateral and palmar face of the digit. The musculocutaneous nerve arises from C6-7 in the rabbit, chinchilla, cat, and pig, from C5-7 or C6-7 in the rat and from C6-7 or C7-8 in dogs. At the shoulder joint the nerve is divided into two branches: the proximal branch, which innervates the proximal portion of the muscle biceps brachii, and the distal branch, which innervates the distal portion of the biceps, the brachialis muscle, and emits the brachial and antebrachial cutaneous medial branches. This nerve may have a distal branch that connects with the median nerve, just below the division of the musculocutaneous nerve into branches.

LUMBAR AND SACRAL PLEXUSES The lumbosacral plexus is an analogue of the brachial plexus. Differences in lumbosacral plexus formations are due to the different segmental participation of certain nerves, as well as their participation in tissue innervation,

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as occurs with the brachial plexus on the periphery. The lumbosacral plexus is formed by nerve roots of the lumbar segments (lumbar plexus) associated with nerve roots of the sacral segments (sacral plexus). However, there is disagreement among authors about the nerves that originate from the lumbosacral plexus, and three possible configurations are mentioned: (i) separately in the lumbar plexus (femoral, cutaneous femoral lateral, obturator, iliohypogastric, ilioinguinal, and genitofemoral nerves) and sacral plexus (ischiadicus, pudendal, and rectal caudal (inferior) nerves), not considering their formation together; (ii) considering only the lumbar nerves and the sciatic nerve as a constituent of the lumbosacral trunk; and (iii) grouping the cranial (superior) and caudal (inferior) gluteus nerves, and tibial and fibular nerves as members of the plexus. Nevertheless, some axon fibers that innervate the pelvic limb via the lumbar and/or sacral nerves could originate from various cord segments, allowing greater participation of each segment in the formation of nerve trunks and terminal nerves. Thus, for the comparison of the innervation of the pelvic or inferior limb it will be considered the formation of unisegmental nerves (first lumbar segments) and the constitution of three consecutive trunks: cranial or superior (middle lumbar segments), medium (last lumbar and first sacral segments), and caudal or inferior (only sacral segments). Components of the lumbosacral plexus spread on the lower extremity, similarly to the way the brachial plexus spreads on the upper extremity. Lumbar nerves spread similarly to nerves from the medial and lateral fascicle of the brachial plexus, and sacral nerves spread similarly to nerves from the posterior fascicle of the brachial plexus. Nevertheless, interest in the details of both plexus formations varies because injuries, as well as variations in the lumbosacral plexus formation, are less frequent in comparison with the brachial plexus. Indications for reconstructive operations of the lumbosacral plexus are exceedingly rare. Lumbosacral structures forming plexus are located at longer distances from each other than the brachial plexus. Therefore, less significant neurological failures develop in the case of injuries of the lumbar and sacral plexuses. Because of the variability of the location of the medullar conus and cauda equine (Table 5.2), occasional lesions cranial to L4-5 produce signs of lumbosacral disease. Disease at the lumbosacral articulations or in the sacrum will produce sensory and motor deficits of the caudal hindlimb (sciatic, cranial, and caudal gluteus), the perineal region (pudendal), and the pelvic viscera (autonomic). A lesion affecting the L4-6 roots, for example, is likely to produce motor or sensory deficit in the extensors and adductor of the thigh (femoral and obturator nerves, respectively), as well as partial effects on the cranial and caudal gluteus nerves. Autonomic innervation to the pelvic viscera is complex. Pelvic visceral tone and contractility are frequently affected by lesions of the lumbosacral plexus; for example, severe

caudal lumbar lesions block central inhibition of micturition and result in urinary incontinence, while the parasympathetic reflex of bladder emptying is usually present. The sympathetic innervation should remain with parasympathetic loss, and detrusor sphincter dysynergy may result in the loss of detrusor muscle activity and the abnormally strong contraction of the urethra sphincter muscle. Lumbar and sacral plexuses play an important role in regional anesthesias, particularly in sacroiliac and pelvic surgery. Epidural anesthesia has been an alternative anesthetic procedure for surgeries caudal to the diaphragm. However, it is known that the administration of drugs into the epidural space also promotes some systemic changes that may be significant in patients. Another important factor to be considered is often the lack of distribution of innervation and the repercussions of the same anesthesia on the sympathetic and parasympathetic nervous systems. Minimally invasive anterolateral or dorsolateral approaches to the lumbar spine are options for the treatment of a number of degenerative spinal disorders. Lumbosacral plexus injuries can occur when exposing the spine and inserting instruments there. Therefore, its location should be considered from the beginning of the approach decision and before the exposure of the lumbar vertebrae. However, the lack of reliable anatomical landmarks on the posterior abdomen presents problems. More anatomical data concerning the lumbosacral plexus in clinical applications are needed in order to prevent lumbosacaral plexus injuries while increasing the safety of lumbar surgery.

Human Lumbosacral Plexus The first portion of the lumbosacral plexus originates from the ventral rami of the L1-4 nerve roots and projects laterally and caudally from the intervertebral foramina, posterior to the psoas major muscle. A communicating branch from Th12, also known as the subcostal nerve, often joins the first lumbar trunk and constitutes a prefixed plexus. Primary divisions give rise to six peripheral nerves: Th12-L1 (iliohypogastric and ilioinguinal), L1-2 (genitofemoral), and L2-L4 (femoral, obturator, and lateral femoral cutaneous). In humans, the medium trunk is formed from L4-5 and S1-3, and can be called the ischiadicus plexus or trunk because all roots constitute the ischiadicus or sciatic nerve that branches into the other nerves to the inferior limb. The ischiadicus trunk emits the proximal branches (superior and inferior gluteus nerves, and two branches to the internus obturator and piriformis muscles) and terminal branches (tibial and common fibular nerves). Finally, the inferior trunk, also called the pudendal plexus, is usually formed by branches from S2-5 and Co1 and gives off the following nerves: perforating cutaneous (S2-3), pudendal (S2-4), rectal inferior (S3-4), muscular branch to the levator ani, coccygeus, and sphincter ani externus (S4), and anococcygeal (S4-5 and Co1).

Comparative Anatomy of the Peripheral Nerves Chapter 5

Nonhuman Primates The lumbar plexus in nonhuman primates originates from L1-4, while the sacral plexus is constituted by L5-6, or L7 when present, and S1-2, being a bifurcated nerve that is the limit between both plexuses (Figure 5.7). This nerve is described in apes (L5) and Cebus (L4); being absent in rhesus macaque, Cynomolgus, and Ateles. In some species, the sacral plexus is divided into sacral and pudendal plexuses. The connection between the lumbar and sacral plexuses almost always occurs in prosimians and primates. There is a functional correspondence between the lumbosacral plexus in humans and some monkeys, although in many cases the medullar segments do not correspond numerically; for example, L1 in humans corresponds to L2 in Macaca. In humans, the first root engaged of the plexus is Th12 or L1, while in apes it is L1, L2 or L3, as observed in chimpanzees and gorillas, whose origin is L2-3. Thus, it can be inferred that the lumbar plexus in apes is formed by the subcostal nerve and L1-3, and has more marked progressive traits than the human plexus. The lumbosacral plexus displays various degrees of pre- and postfixation. This situation is due to the number of presacral vertebrae and probable shortening of the thoracic region. The prefixation process is more pronounced in orangutans and other primates who have suffered a reduction in the presacral vertebral column, whereas the postfixed condition is the result of the stretching of this portion. Thus, the presence of 13 thoracic vertebrae is considered a primitive feature to primates, based on the presence of this number of vertebrae in arboreal shrews considered the common ancestor of all primates. Likewise, the number of six lumbar vertebrae is the original condition in primates, having observed the Plathyrrhinos, Alouattinae, Atelinae, and higher primates. Regarding the number of sacral vertebrae, this was equal to three in primate ancestors, although currently the average number may vary from three to six; in most current primates there are three. Thus it appears that there is a tendency for the inferior displacement of the lumbosacral plexus in all primate genera except the Hominoidea, featuring a postfixed plexus. In the prefixed plexus, the last thoracic nerve or subcostal (Th12 or Th13) participates in the formation of the lumbar plexus, while in the postfixed one is the constant presence of S3. In long-tailed monkeys (Haplorrhini), the coccygeal and caudal nerves are interconnected to form a side length on each side of the tail, as occurs in Ateles, which has eight coccygeal spinal segments involved in the innervation of the tail. Also, the displacements of bones change the number of roots and the nerve topography, causing a relationship between the plexus structure, lower limb development, and body posture. The lumbosacral plexus nerves are classified according to their distribution in flexor (iliohypogastric, ilioinguinal,

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genitofemoral, anterior branches of the femoral, obturator, flexor branches of the tibial and common fibular, puboischio-femoral moral, and pudendal nerves) and extensor nerve groups (lateral femoral cutaneous, femoral, piriformis, superior and inferior gluteal, sciatic, and posterior femoral cutaneous nerves). However, functionally, the lumbosacral plexus does not provide a distinct division between the flexor and extensor nerves in primates, because nonhuman primates have lower limbs of pickup and carrier type compared to humans who have only the carrier type limb. Iliohypogastric, ilioinguinal, and genitofemoral nerves almost always occur in prosimians and all primates, and they may originate from the lumbar plexus (primates) or separately (prosimians). However, in apes, in general, the ilioinguinal nerve is absent, which is probably due to the shortening of the thoracic region and decreased number of nerves in the lumbar segment. Also, in apes, and particularly in the gibbon, a similarity is observed to the upper lumbar nerves organization in humans. However, in this species L1 and L2 do not form a common trunk for the iliohypogastric nerve, as in humans, whereas Th12-L1-2 in the chimpanzee and orangutan, and L1-3 in the gorilla, are joined together and form this nerve and the genitofemoral nerve, which in the gibbon appears from L2. In addition, in the Hominoidea (apes and gibbon), the lateral femoral cutaneous nerve arises from the union of L2-3. However, in Cebus and Ateles the iliohypogastric, ilioinguinal, and genitofemoral nerves originate from the union of Th12 and L1, while the lateral femoral cutaneous nerve arises from L2-3, but in both species these nerves do not belong to the lumbar plexus. Except for the Cynomolgus and rhesus macaque, whose lumbar and sacral plexus are formed by a single unit from L1-7-S1-2, and Ateles, which is formed from L3-5 and S1-2, in other primate species described here distinct lumbar and sacral plexuses are observed. The lumbar plexus in chimpanzees, orangutans, and gorillas is formed from L2-3, while the sacral plexus emerges from L5-6 and S1-2, and is joined by the bifurcated nerve (L4). However, in the gibbon the lumbar plexus arises from L2-4 and the sacral plexus from L5-S1-2, as in humans. In Cebus, the lumbar plexus arises from L3-4 and the sacral plexus from L5-S1 and the bifurcated nerve is in L4, and there is a coccygeal plexus originating from S2-5-Co1-2. In monkeys, the lumbar plexus gives rise to the femoral and obturator nerves and, in some cases, the lateral femoral cutaneous nerve (mentioned earlier). The femoral nerve arises from L2-3 in the gibbon, but presents a more cranial origin in the chimpanzee and orangutan, emerging from L1-3. This nerve arises from a common trunk with the obturator nerve in the gorilla (L2-4), rhesus and Cynomolgus (L3-5), Cebus (L3-4), and Ateles (L2-3). In rhesus and Cynomolgus, an inferior femoral nerve is described originating from L5-6. In gibbons, chimpanzees, and orangutans the

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PART I History, Histology and Development of the Peripheral Nerves

FIGURE 5.7 Ventral view of the lumbar, sacral, and coccygeal plexuses of Cebus or Sapajus apella. L2 to Co3 correspond to the spinal cord segments. Second lumbar nerve (NL2; medial branch of L2 - L2mb); cutaneous femoral lateral nerve (CFL); third lumbar nerve (NL3; medial branch of L3 - L3mb and lateral branch of L3 - L3lb); fourth lumbar nerve (NL4; medial branch of L4 - L4mb, intermedium branch of L4 - L4ib, and lateral branch of L4 - L4lb); fifth lumbar nerve (NL5); femoral nerve (F); obturator nerve (O); lumbosacral trunk (LSt); ischiadicus nerve (Is); first sacral nerve (NS1); second sacral nerve (NS2; medial branch of S2 - S2mb and lateral branch of S2 - S2lb); third sacral nerve (NS3; medial branch of S3 - S3mb and lateral branch of S3 S3lb); fourth sacral nerve (NS4); fifth sacral nerve (NS5); pudendal nerve (Pud); first coccygeal nerve (NCo1); second coccygeal nerve (NCo2); third coccygeal nerve (NCo3); major coccygeal nerve (MCo) and unpaired coccygeal nerve (Coi). Reproduced, with permission, from Barros, Prada, Silva, Ribeiro, and Silva (2003).

Comparative Anatomy of the Peripheral Nerves Chapter 5

obturator nerve emerges from the L3-4, L2-4, and L1-2, respectively. A lumbosacral trunk is formed both in humans and in nonhuman primates, which shows a slight asymmetry between the right and left antimers. In apes, except for the chimpanzee, the prefixed lumbosacral trunk is formed by L4-5-S1-2, The degree of pre- and postfixation of the plexus in the other species varies according to the first or last root involved in their formation. Thus, in the chimpanzee and Ateles the trunk is formed by L3-5-S1-2, while in rhesus it is formed from L4-6-S1-2, and in Cynomolgus it is formed by L5-7-S1-2. However, in Cebus a lumbosacrococcygeal trunk is described constituted from L2-5-S1-5-Co1-3, with prefixation in L1 and postfixation in L5. The short branches of the lumbosacral trunk (piriformis, obturator internus, iliopsoas, pubo-ischio-femoral, gluteus, and tensor of the fascia lata) emerge directly from the trunk or from the long nerves (sciatic, caudal femoral cutaneous, tibial, and common fibular nerves). The piriformis nerve emerges from L4-S1 in the anthropoid, L7-S1-2 in rhesus, L6-7 in Cynomolgus, L5-S1-2 in Ateles, and as plexus branches in Cebus. Concerning the short nerves, the three gluteus nerves (superior medium and inferior) are very important; they arise from the union of L4-5 in Cebus, L4-S1-2 in Ateles, L3-4 in apes, and as a branch of the sciatic nerve in rhesus and Cynomolgus. In some Hominoidea primates, a pubo-ischiofemoral nerve is observed that has its origin from L3-4-S1 in the chimpanzee, L4-S1 in Ateles, and L5-7 in rhesus and Cynomolgus. In these species the pubo-ischio-femoralis nerve runs very close to the nerve of the flexor muscles and innervates the pubo-ischio-femoral, gemelli, internal obturator, and quadratus femoris muscles. As to the sciatic nerve, in most of the nonhuman primates the presence of a typical sciatic nerve is not observed; it is represented by the common fibular and tibial nerves originating directly from the lumbosacral trunk. Thus, a typical sciatic nerve is observed in Cebus, which originates from the L4-5-S1-2, subsequently dividing into the common fibular and tibial nerves. However, in rhesus and Cynomolgus three possible sources for this nerve are observed: from L5-S1-7 in prefixed plexuses, from L6-7-S1-2 in postfixed plexuses, and from L5-S1-6 in animals with six lumbar vertebrae, with the common fibular nerve originating from L5-7 and the tibial from L5-7-S1-2. In the chimpanzee and orangutan, the sciatic trunk is described formed by L3-4 and receiving fibers from S1 to form the common fibular nerve or S1-2 for the tibial nerve. In the gorilla and gibbon, the sciatic trunk divides into the common fibular nerve formed by L4-5-S1 and tibial nerve (L4-5-S1-2), whereas in Ateles the trunk is formed from L3-4-S1-3, constituting the common fibular nerve, and from L3-4-S1-2, the tibial nerve. In nonhuman primates the formation of a pudendal plexus as in humans is not observed, and this emerges from the lumbosacral trunk in Cebus (S1-3), Ateles (L4-S1-3),

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rhesus monkey, Cynomolgus (L7-S1-2), and anthropoids (S2-3). In Cebus, Ateles, rhesus, and Cynomolgus, the final portion of the sacrococcygeal plexus, the nerves arise from the tail, which is quite important in these species as it is used in locomotion and prehension of objects that innervate a developed coccygeal musculature.

Other Mammals As mentioned in the section on the brachial plexus, different experimental models can be employed in the study of injury to peripheral nerve fibers, mimicking the different conditions of injury in humans. Among the methods widely studied are those that produce mechanical trauma, with special reference to the sciatic nerve. In rodents, rabbits, and domestic mammals it can be inferred that, as in nonhuman primates, the more cranial lumbar innervation does not arise through the formation of a common trunk as in humans. The more cranial lumbar ventral rami (L1-4) run individually, constituting the iliohypogastric (L1), ilioinguinal (L2), lateral femoral cutaneous (L4), and genitofemoral (L3) nerves, the latter relying on a contribution from L4. On the other hand, in the prefixed plexus of rabbits and rodents, with the exception of the guinea pig and chinchilla, the iliohypogastric nerve receives a contribution from Th13 and the ilioinguinal nerve arises from L1-2. In species that have seven lumbar segments (carnivores and swine), there are two iliohypogastric nerves, cranial and caudal. The latter arises from the ventral branches of the L1-2, and the ilioinguinal nerve arises from the ventral branch of the L3. The chinchilla (Figure 5.8), in turn, has six lumbar segments, the L1-2 spinal nerves originate the cranial and caudal iliohypogastric nerves and the ilioinguinal nerve arises from L3, while in the guinea pig the iliohypogastric nerves emerge from L4. The formation of the genitofemoral and lateral femoral cutaneous nerves in various domestic mammals has been described as follows: in the guinea pig and rat both nerves arise from L3-4; in the rabbit from L4-5; in the dog, the lateral femoral cutaneous nerve arises mostly from L4, and occasionally there might be contributions from L3 or L5, and the genitofemoral from L3-4; in the cat, the lateral femoral cutaneous nerve arises from L4-5 and the genitofemoral nerve arises from L3 as in the chinchilla and pig. In both these species the lateral femoral cutaneous nerve emerges from L4. The iliohypogastric nerve emerges between the psoas major and minor muscles and innervates the abdominal wall, paralumbal fossa, and peritoneum; while the ilioinguinal and the genitofemoral nerves, after emerging between the lumbar muscles, extend subperitoneally and in a caudoventral direction toward the annulus inguinalis abdominalis. These nerves innervate the internal abdominal oblique muscle and the cremaster muscle, the testicular fascia, spermatic funiculus and preputium in

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FIGURE 5.8 Ventral view of the vertebral column to show the spinal roots of the lumbosacral plexus in the chinchilla. (a) The unisegmental nerves are shown: cranial iliohypogastric (Ihcr) from L1; caudal iliohypogastric (Ihcd) from L2; ilioinguinal (Ii) and genitofemoral (Gf) from L3; lateral cutaneous femoral (Cf) from L4; the plurisegmental nerves, obturator (O) and femoral (F), originated from the union of L4 and L5; and pudendal (Pd) from the joint of S1-2. The emergence of the ischiadicus plexus (P) from L5-6 and S1 is also shown. (b) Detail of the vertebral column (ventral view) to show the spinal origin of the following nerves: obturator (O), femoral (F), pudendal (Pd), rectal caudal (R) originated from S2-3, and the origin of the ischiadicus plexus (P). Scale bar: (a) ¼ 1 cm; (b) ¼ 1.5 cm. Reproduced from Martinez-Pereira and Rickes (2011).

males, the mammae in females, and the skin of the medial side of the femoral region in both sexes. The lateral cutaneous femoral nerve arises from the plexus and projects toward the caudal iliac region by crossing the abdominal muscles and innervates the external abdominal oblique, iliac, and tensor fasciae latae muscles, the skin of the femoral region, and the craniomedial side of the knee joint. It has been reported that the lumbosacral plexus is formed by the union of L3-7 and S1-3 in dogs (Figure 5.9), T13, L1-6 and S1-S2 in rats, L4-7 and S1-3 in cats and rabbits, L3-6 and S1-3 in guinea pigs, L4-6 and S1-3 in Chinchilla, and L4-6 (7) and S1-2 in pigs. In all these species the lumbosacral plexus originates two trunks: cranial (responsible for the formation of the femoral and obturator nerves), and caudal (from which emerge the other nerves). The constitution of the cranial trunk is variable among the species described. This stems from the presence of more caudal lumbar and/ or sacral segments in the formation of the obturator nerve of the guinea pig (L5-6) and rabbit (L5-S3). However, in the rat the cranial trunk is formed by L2-4 or L5, but the femoral nerve originates from L2-4(5) and the obturator arises from (L2)L3-5, while in the dog, pig, and chinchilla both nerves emerge from the same trunk formed by L3-6

and L3-4, respectively. The femoral nerve arises from L45 in the guinea pig, mostly from L6 with contributions from L5 and L7 in rabbits, and from L5-6 and the obturator nerves emerges from L6-7, both in the cat. The femoral nerve emerges between the psoas major and minor muscles to innervate them, and together with the deep lumbar muscles, reaches the femoral space and emits branches to the femoral quadriceps muscle. Lower down arises the saphenous nerve that innervates the gracilis, pectineus and sartorius muscles, branching to supply the skin and fascia in the medial femoral region. The obturator nerve, after leaving the pelvic cavity through the obturator foramen, supplies the branches of the adductor, pectineus, gracilis, and internal and external obturator muscles. The caudal trunk, which gives rise to the nerves innervating the pelvic limbs, is reportedly formed by the union of L6-7 and S1-2 in dogs, L4-7 and S1-2 in cats, L6 and S1-2 in guinea pigs, L5-7 and S1-3 in rabbits, and L5-6 and S1-2 in the pig and Chinchilla (Figure 5.10). However, in the rat it is described that L4 and L5 always, and L6 rarely, contribute to the formation of the common root, or that L4-6 and S1-2 are contributing to this trunk. In this chapter, the common caudal trunk is referred as the ischiadicus

Comparative Anatomy of the Peripheral Nerves Chapter 5

L5

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S3

L7 S1

10

1

3 4

2

8⬘ 8

9

5 1⬘ 1⬘⬘ 6⬘ 6

FIGURE 5.10 Ventrolateral view of the nerves originating from the common root, which is formed by the union of the L5-6 and S1 spinal nerves, and constitute the ischiadicus plexus (P) in the gluteal region and posterior limb of Chinchilla. This plexus is formed by the following nerves: cranial gluteal (Gc), caudal gluteal (Gd), caudal cutaneous femoral (Cfd), and ischiadicus (Is). The ischiadicus nerve is divided into cutaneous surae caudalis (arrow), cutaneous surae lateralis (Csl), common fibular (Fc), and tibial nerve (T). Scale bar: 1 cm. From Martinez-Pereira and Rickes (2011).

7 7⬘

6⬘⬘ 6⬘⬘⬘

7⬘⬘ 7⬘⬘⬘

FIGURE 5.9 Lumbar and sacral nerves of the dog, medial view. 1 femoral nerve (10 , femoral quadriceps branches, 100 saphenous nerve), 2 obturator nerve, 3 pelvic nerve, 4 branches of the internus obturator, gemelli, and quadratus femori muscles, 5 ischiadicus (sciatic) nerve, 6 common fibular nerve (60 cutaneous surae lateralis nerve, 600 superficial fibular nerve, 6000 profound fibular nerve), 7 tibial nerve (70 cutaneous surae caudalis nerve, 700 plantaris medial nerve, 7000 plantaris lateralis nerve), 8 pudendus nerve (80 profound perineal nerve), 9 cutaneous femoral caudal nerve, and 10 rectal caudal nerve. Reproduced, with permission, from Dyce et al. (2009). Textbook of veterinary anatomy. 4th ed. Elsevier, 2009.

plexus, because this constitutes a common root, originating from different spinal nerves and branched into the following nerves: cranial gluteus, caudal gluteus, caudal cutaneous femoral, and ischiadicus. The ischiadicus plexus covers the iliac region dorsocaudally, reaching the femoral

region caudally and ramifies into their four branches. On the other hand, some peculiarities of each nerve and species can be considered. First, the origin of the cranial gluteus nerves varies in all species, being formed from L6 and S1 in the guinea pig, from L4-6 and S1 in rats, from L6-7 in cats, or from a common root with the caudal gluteus in rabbits (L6-7) and pigs (L5-6 and S1). However, both cases are described in dogs: the cranial gluteal nerve arises only from L6-7-S1 or both nerves arise from L6-7-S1 and in the chinchilla it is described that both nerves originate from the ischiadicus plexus. The cranial gluteal nerve, after leaving the pelvic cavity through the incisura ischiadica major, supplies the branches of the gluteus profundus, piriformis, and tensor fasciae latae muscles. Second, as to the caudal gluteal nerve, when it originates alone it is reported to arise from L7 in dogs, from S1 in the guinea pig, while in rats it arises from the peroneal nerve (L6-S1-4-Co1-2). The caudal gluteal nerve is a motor nerve arising from the caudal portion of this common trunk and innervates the gluteus superficialis, the cranial part of the biceps femoris, the abductor cruris caudalis, and the vertebral head of semitendinosus and semimembranosus muscles. The gluteaus medius is innervated by the two gluteal nerves. Third, the caudal femoral cutaneous nerve in the guinea pig originates from the sciatic nerve and then separates from it; in dogs it arises mostly from L4 with contributions from L3 and L5; in the cat from S2-3. The caudal cutaneous femoral nerve innervates the biceps femoris and semitendinosus muscles, and then between these muscles, supplies the skin over the tuber ischiadicum, the caudal portion of the femur and, through a union with the pudendal nerve, the perineum.

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Considering the variation in the number of lumbar and sacral vertebrae, the nerve roots that form the ischiadicus nerve are distinct for different species but it should be noted that these represent the last spinal nerves forming the plexus, being different from the roots of the ischiadicus plexus in the cat (L6-7 and S1-2) and rat (L4-6). The sciatic nerve is the largest nerve in the body, often suffering injuries that result in insensibility and motor dysfunction in all regions of the affected limb. The ischiadicus nerve ramifies into the proximal muscular branch for the obturatorius internus, gemelli, and quadratus femori muscles. This branch extends to the skin after innervating the caudal portion of the biceps femoris muscle, semitendinosus and semimembranosus muscles, before diverging into the tibial and the common fibular nerves after forming the cutaneous surae lateral and caudal nerves. The cutaneous surae lateralis nerve, the first branch of the ischiadicus nerve, innervates the hypodermis and skin in the cranial surae region, while the cutaneous surae caudal nerve crosses the caudal sural region and innervates the skin of this region and the common calcaneal tendon. The tibial nerve crosses to the tarsal joint level, emitting slender branches to the skin in this region, and divides into the digitalis dorsalis and plantaris communis nerve V. After this branch, the tibial nerve supplies a distal muscular branch, which extends to the flexor muscles, between the two heads of the gastrocnemius and popliteus muscles, and continues as branches to the muscles of the plantar surface of the metatarsus and divides into the digitalis plantaris communis nerves II, III, and IV. The common fibular nerve passes over the gastrocnemius muscle and enters the sulcus between the peroneus longus and extensor digitorum lateralis muscles, then dividing into the superficial fibular and profound fibular nerves. The superficial fibular nerve innervates the skin of the dorsum of the tarsus and metatarsus and emits the muscular branches to the tibialis cranialis, extensor digitalis longus and extensor digitalis lateralis muscles, and forms the digitalis dorsalis communis III and IV nerves. The profound fibular nerve innervates the fibularis longus and fibularis brevis muscles. The pudendal plexus is described only in rats, being formed by the union of L6, S1-4, and Co1-2 of the cranial gluteus nerve. However, the pudendal and caudal rectal nerves originate together in the guinea pig (S2-4), in rabbits (S1-4), dogs (S1-3). and cats (S2-3), while in the chinchilla both nerves emerge separately from S1-2 (pudendal) and S2-3 (rectal caudal), as well as in the pig, in which they emerge from S2-3 (pudendal) and S4 (rectal caudal). The pudendal nerve crosses toward the caudal pelvic aperture where it divides into the dorsal nerves of the penis or clitoris, superficial and profound perineal. The former innervates the ischiocavernosus, bulbospongiosus, and retractor penis muscles, and the preputium in males and the constrictor vulvae muscle, clitoris, and vulva in females. The

superficial and profound pudendal nerves innervate the skin and muscles of the anal and perianal regions. The rectal caudal nerve innervates up to the end of the rectum, the sphincter muscles of the anus, and the skin of the anal region.

BIRDS Unlike the spinal cord of mammals, the spinal cord of birds extends along the whole length of the vertebral canal, including the coccygeal region, and its length is equal to the whole vertebral column and decreases in diameter caudally. Although its segmentation is the same as in mammals, the cervical portion is longer and variable across the avian species, while the thoracic portion is very short and the sacral cord is also longer, such as in the coccygeal region. Two intumescences—cervical and lumbar—are observed in birds, and only birds display a glycogen body, lying in the spinal cord in the area of its lumbosacral sinus. Glycogen body cells are of glial origin, possibly astrocytes, having undergone extreme differentiation, but neither the origin of these cells nor the function of the glycogen body has been entirely clarified.

Brachial Plexus The avian brachial plexus has been the subject of several clinical and surgical studies particularly in wild and migratory birds. Plexus components are frequently involved in traumatic episodes, in local and regional anesthetic procedures, and in studies to determine the functional role of red and white fibers during the flight of poultry. The brachial plexus innervates the muscle of the wing and trunk as well as the blood vessels of this region of the avian body. The brachial nerves, which contribute to the plexus, depart from the cervical intumescence of the spinal cord at the cervicothoracic junction (Figure 5.11). The plexus has four roots, which unite to form three short trunks, where there is an exchange of fibers. The trunks can divide into dorsal and ventral divisions, which combine to form two nerve cords. Branches from the dorsal cord supply the dorsal compartment (extensor muscles) and the overlying skin of the limb muscles, while branches from the ventral cord innervate the flexor muscles of the wing. However, some differences are observed across avian species. In the chicken the last three cervical (C13-15) and the first two thoracic (Th1-2) nerves constitute the brachial plexus, while in the duck and goose the last two cervical and the first two thoracic nerves form that plexus, and in the turkey the brachial plexus is formed by C12-13 and Th1-2, constituting three trunks. However, in the pigeon the brachial plexus is formed by spinal segments 13 to 16, which correspond to the three last cervical and the first thoracic nerves. Still, in these animals there is a secondary plexus comprised of the union of the twelfth and thirteenth

Comparative Anatomy of the Peripheral Nerves Chapter 5

FIGURE 5.11 Ventral view of the right wing of Columba livia. Shown are the distributions and pathways of the ventral cord (Vc) and dorsal cord (Dc). The dorsal nerves to the dorsal surface of the wing are the axillary (A) and radial (R). The Vc is divided into median-ulnar nerve (MU), caudal cutaneous brachial nerve (arrowhead), and pectoral trunk (PT). In the elbow joint, the MU separates into the ulnar (U) nerve and median (M) nerve, which emits the musculocutaneous branch (arrow). Adapted, with permission, from Franceschi, Souza, Provenci, and Martinez-Pereira (2009).

spinal segments. In the eastern screech owl (Otus asio) the plexus is formed by C12-15 and Th1, while in the great horned owl (Bubo virginianus) the major contributors to the plexus are from C11-13 and Th1. In some raptors there is an accessory brachial plexus that consists of contributions from the two or three most caudal dorsal nerve roots. The roots form three trunks in domestic birds and four trunks in raptors, which constitute the dorsal and ventral cords. The terminal branches of the ventral cord are the pectoral trunk and the median-ulnar nerve, while the dorsal cord issues the axillary nerve and continues inside the wing as the radial nerve. Functionally, the plexus can be divided into four groups: dorsal and ventral thoracic nerves, and dorsal and ventral brachial nerves. The dorsal thoracic nerve innervates the superficial and profundus rhomboideus muscles and the ventral and superficial serratus muscles. The ventral thoracic nerve innervates the supracoracoideus and scapulohumeral muscles, and originates the subscapularis nerve. It also originates the large pectoral nerves that innervate the pectoral muscles. A filament of the brachial dorsal nerve innervates the longissimus muscles of the dorsum, and another filament forms the axillary nerves, sending branches to the skin of the dorsal side of the wing and shoulder, for the deltoideus, coracobrachialis, and propatagialis cervical muscles. The anconeal (which innervates the triceps muscle through its profound branch and supplies the anconeus muscle through a superficial branch) and radial nerves are also part of the group of dorsal brachial nerves. The radial nerves are thick filaments innervating a head of the humero-brachial and triceps muscles. At the junction of the elbow, the radial nerve sends two branches to the extensor carpi radial and supinator

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muscles and a third to the joint, which is further divided into cranial (innervating metacarpal and digital regions with branches to the abductor digital longus, extensor digital longus, and small metacarpal extensor muscles) and caudal branches (extensor carpi ulnaris, extensor digitali communis, epicondyle-ulnar muscles, and wing). The ventral brachial nerves include the caudal cutaneous brachial nerves and the median-ulnar nerve. The latter nerve crosses the medial side of the humerus and gives a branch to the coracobrachialis muscle and another to the brachial biceps muscle. At the level of the elbow joint the ulnar and median nerves are separated and the ulnar innervates the extensor aspect of the joint, giving rise to branches of the flexor carpi ulnar muscles, which are divided into cranial (innervating the superficial digital flexor muscle and small metacarpal flexor muscles) and caudal (running along the surface of the carpal and metacarpal regions and reaching the digits) branches. The median nerve crosses the elbow joint and then courses more distally along the medial surface of the brachial and metacarpal regions, forms the cutaneous nerves, and innervates the flexor carpi radial and pronator teres muscles by a musculocutaneous branch, the ventral ulnar metacarpal, superficial, and profound digital flexor and small metacarpal muscles.

Lumbar, Sacral, and Pudendal Plexuses The innervation of the pelvic region, hindlimb, and tail is accomplished by the mixed nerves that constitute the lumbar, sacral, and pudendal plexuses. Among the nerves present in these regions, the ischiadicus nerve is very important for the diagnosis of Marek’s disease. One of the most widespread avian infections, this pathology causes a swelling of peripheral nerves, loss of striated mass, and lethargy. Before describing the innervation of the pelvic region, hindlimb, and tail, it is important to note that the caudal region of the vertebral column is much differentiated in birds. It is formed by 14 to 15 vertebrae, depending on the species, which are fused constituting the synsacrum. The connection between the synsacrum and the ilium bone, which reaches far into the thoracic region, is highly important for the shape of the trunk in birds. The bony connection is accomplished cranially by spines and transverse process and caudally by the transverse process of the synsacrum, which are fused into a continuous bony plate that permits the passage of nerves and blood vessels. Going from cranial to caudal the following vertebrae in the synsacrum are differentiated: synsacrothoracic, synsacrolumbar, primary sacral, and synsacrocaudal. If we consider that the lumbar to coccygeal segments of the spinal cord are located in the canal of the synsacrum, the spinal nerves arising from it can be called synsacral nerves (Sy). The lumbar plexus is described as formed by the two last lumbar ventral (L6-7) and one sacral (S1) strands, also called the forked nerve (furcalis), that connects the lumbar plexus to

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the sacral plexus. The sacral plexus is formed by the ventral strands of the spinal nerves S1-S5(6), and the number of roots forming the plexus ranges from five to seven. The sacral plexus also communicates with the pudendal plexus (S9-12) through the bigeminus nerve. The pudendal plexus innervates the ventral muscles of the tail, the muscles of the cloaca, and the skin in both regions. Nevertheless, sometimes the furcal and bigeminus nerves may not be visible. In the sacral plexus the roots unite to form three trunks: (i) cranial (formed by the first three roots); (ii) medium (fourth root alone); and (iii) caudal (fifth and sixth roots united). However, these descriptions refer to domestic birds (chicken, duck, and goose). In the ostrich (Struthio camelus) the lumbar plexus is formed by the union of four roots (Sy2-5), while the sacral plexus is formed by the union of seven roots (Sy5-11). Sy5-9 form the cranial trunk of the plexus, Sy10-11 constitute its caudal trunk and Sy5 constitutes the forked nerve. However, in the Kyrgyz pheasant (Phasianus colchicus mongolicus) the sacral plexus sacralis is formed by the ventral branches of S1-5 and is located between the lumbar and pudendal plexuses. In this species, the sacral plexus originates three trunks: a cranial trunk formed by the union of S1-3, a medium trunk formed by S4, and a caudal trunk comprising S5 only. The cranial and medium trunks connect in a single root. The nerves of the lumbar plexus are iliohypogastricus and ilioinguinalis (both to the ventral muscles of the trunk), obturator (external obturator and adductors muscles), cutaneous femoris (to the sartorius muscles and cutaneous branch in the lateral surface of the thigh), femoral (the thickest branch of the plexus that innervates the iliac, quadriceps femoris or femorotibialis, gracilis, and tensor fasciae latae muscles), cranial gluteus (medius and profound gluteus muscles), and saphenous (innervates the knee joint and the inner surface of the shank). However, in the ostrich the cranial femoris nerve originates from the union of Sy2-3, supplies the iliotibialis cranialis muscle, and divides into lateral and cranial femoral cutaneous nerves that supply the skin of the lateral and cranial surface of the thigh. The obturator nerve is the smallest branch of the lumbar plexus formed by Sy3-5 in the ostrich, while in the chicken it is formed by two lumbar roots. The sacral plexus nerves include caudal gluteal (superficial gluteus and biceps femori); nerve branches to the biceps femori, semitendinosus, semimembranosus, quadratus femori, and gemelli muscles; caudal cutaneous femoris (skin of the caudal surface of thigh); and ischiadicus nerves. The ischiadicus nerve, the largest nerve of the plexus, arises from S1-4 in domestic birds and the Kyrgyz pheasant, and from Sy5-9 in the ostrich. The nerves originating from the ischiadicus nerve are the cutaneous cruris lateralis (skin of the lateral aspect of the tibiotarsus, not described in domestic birds, present only in the ostrich); the tibial (larger terminal branch of the ischiatic, which bifurcates to form the suralis medialis and lateralis nerves to supply the flexor muscles

of the leg and toes); the medial tibial nerve (that innervates the gastrocnemius and popliteus muscles, then continues as the parafibularis and plantaris medialis); and the fibular nerve, which is divided into superficial fibular (supplies the extensor brevis digiti II, fibularis longus, fibularis brevis, extensor digiti III and IV brevis muscles); and the profound fibular (continues as the metatarsalis dorsalis medialis nerve and innervates the extensor hallucis longus and abductor digiti II).

REPTILES AND AMPHIBIANS The reptilian spinal cord extends throughout the entire length of the vertebral canal, filling only 50% of the lumen in alligators and 29-34% in several lizard species. Although the reptilian spinal cord has a segmented organization as in other vertebrates, it lacks some of the functional regionalization seen in mammals. Because of the wide variation in the number of vertebral segments across taxa and the lack of distinct regional boundaries, spinal segments are typically numbered from the first cervical segment on caudally, and the mammal-based nomenclature for the spinal cord segments is not always applicable to the reptiles. The reptilian spinal cord tends to be larger near the brain stem, and the cervical and sacral regions are enlarged in cross section, corresponding to the brachial and lumbosacral plexuses, although a lumbar region is absent in turtles, lizards, and crocodiles. In snakes and limbless lizards, cords lack the brachial and sacral intumescences. The organization of the spinal cord is similar to other vertebrates. The white matter comprises myelinated axons and connects the brain stem to the rest of the cord by long bundles of ascending and descending nerve fibers. The gray matter is organized in dorsal and ventral horns (input and output roots), and varies relatively little in total cross-sectional area along the cord in lizards and turtles. No lateral horn can be distinguished, but the large area of gray matter between the horns is comprised of interneurons. In chelonians, the ventral horn is reduced in the midtrunk because of fewer motor neurons associated with the lack of trunk musculature. The PNS includes laterally paired spinal nerves, although the extent of the dorsal and ventral roots varies along the cord and between species, as a function of variations in vertebrae number. The control of the limbs is accomplished by the cervical or brachial plexus and the sacral (or lumbosacral) plexus. The brachial plexus is formed by the more caudal cervical spinal nerves, which innervate the shoulder and forelimb muscles and may send branches to the respiratory muscles. The brachial plexus presents a similar organization to that of birds, comprising three trunks that form the dorsal and a ventral cords. In painted turtles or terrapins and tortoises the brachial plexus is formed by C6-8 and Th1, while in five species of Crocodylia (Alligator

Comparative Anatomy of the Peripheral Nerves Chapter 5

mississippiensis, Crocodylus siamensis, C. acutus, Osteolaemus tetraspis, and Gavialis gangeticus) the plexus generally is comprised of the seventh to eleventh spinal nerves (SN). The ventral cord is derived from ventral divisions of SN(7)8-10(11) and gives rise to a large number of nerve branches by the supracoracoideus, median-ulnar, and ventral brachial cutaneous nerves that innervate the flexor or ventral musculature of the brachium and antebrachium, with the exception of the humeroradialis muscle. Similarly, the dorsal cord is derived from dorsal divisions of SN(7)810(11) and divides into the axillary and radial nerves, which supply most innervation of the remaining extensor musculature. However, the majority of the forelimb muscles receive innervation from more than one branch of the plexus. Briefly, the brachial inferior nerve divides to form the superficial radial nerve and the deep branch of the radial nerve to the shoulder and dorsal forelimb. The median nerve innervates the ventral and flexor surface of the limb, while the supracoracoideus, subscapular, and ulnar nerves innervate the pectoral, subscapularis, and ventral forelimb muscles, and the deltoideus nerve innervates the shoulder. The description of the lumbosacral plexus is based on studies in iguana (Iguana iguana), varanus (Varanus dumerilii), turtles, and the red-foot tortoise (Geochelone carbonaria). The lumbosacral plexus is formed by SN23-28 in the iguana and SN27-31 in varanus. Nevertheless, it is important to note that these animals have 24 presacral and 2 sacral vertebrae and 29 presacral and 2 sacral vertebrae, respectively. The lumbosacral plexus is constituted by three trunks: a cranial trunk formed by SN23-24 in the iguana and by SN27-28 in the varanus; a medium trunk or sacral plexus (from SN25-27 in the iguana and from SN28-30 in the varanus); and a caudal trunk (from SN27-28 in the iguana and from SN30-31 in the varanus). The cranial trunk originates the femoral and obturator nerves and two nerve branches to the abdominal wall. From the medium trunk arise four nerves: dorsal (fibularis or peroneus), ventral (tibial), ventralmost (pubo-ischio-tibialis) nerves, and the thin caudoiliofemoralis nerve. The fibularis nerve innervates the calf and foot extensor muscles, and the tibial nerve supplies the flexor muscles of the same region. The pubo-ischio-femoral nerve can be analogous to the ischiadicus nerve described in other vertebrate species, mainly considering their innervation territories (laterocaudal surface and muscles of the thigh, including the flexor muscles of the tibia and the pelvic muscles, with the exception of the obturator nerve’s territory). The caudal trunk of the lumbosacral plexus forms the caudofemoralis, pudendal, and caudoischiadicus nerves and the innervation to the musculature of the caudal body wall. The pudendal nerve has a wide innervation territory, including the cranial pudendal (muscles of the tail) and caudal pudendal (muscles of the penis and cloaca) divisions. In turtles the lumbosacral plexus arises from Th8-10 and S1-2, comprising eight or nine spinal nerves scattered in the

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skin and musculature of the thigh. However, in the red-foot tortoise three origins of the lumbosacral plexus are described: T6-S5, T6-Ca1, and S1-5. The ischiadicus nerve of both species arises from the Th10-S1-2 and it divides into three ischiadicus nerves in the turtle. The second arrangement (T6-Ca1) of the apparent origin of the nerves (T6-S5) exhibits no involvement of nerve roots from the caudal and/or pudendal plexuses in the red-foot tortoise. This finding may reveal that the functional significance of the involvement of a caudal and/or pudendal plexus in this species is questionable and is very important to anesthesia practice in chelonians. In amphibians, the adaptation to terrestrial life involved the development of limbs and CNS modifications subserving tetrapod locomotion. Nevertheless, some species are limbless (the caecilians of order Gymnophonia) or possess rudimentary extremities (e.g., Amphiuma, a genus of aquatic salamanders). The spinal cord varies across amphibians, being more differentiated in anurans than in urodeles. Anurans have a relatively short spinal cord with 11 segments and conspicuous intumescentia cervicalis and lumbalis. The spinal cord terminates in a relatively long and slender cone, which represents the remnant of the caudal portion premetamorphosis. The brachial plexus is originated by SN2-3 in anurans and constitutes two cords that form the brachial, radial, and median-ulnar nerves for the limb musculature. SN7-10 join to form the lumbosacral plexus, whose main component is the ischiadicus nerve, which originates the iliohypogastric, femoral or crural, tibial, and coccygeal nerves. However, in the Japanese giant salamander (Megalobatrachus japonicus) the lumbosacral plexus is comprised of SN19-22 (SN20 is a bifurcated nerve). In this species, the nerves are organized in four groups: (i) nerves that innervate the caudofemoralis muscle (SN19-21, peroneus, or common fibular and tibial nerves); (ii) nerves passing between the caudofemoralis and caudoischiadicus muscles (SN20-22, pubo-ischio-tibialis, and pudendal nerves); (iii) nerves that follow ventrally to the caudoischiadicus muscle (SN21-22 and nerve to the caudoischiadicus muscle); and (iv) terminal nerves of the limb (ischiadicus from SN20, femoral from SN19-20, and obturator from SN19-20).

FURTHER READING Akita, K., 1992a. An anatomical investigation of the muscles of the pelvic outlet in Japanese giant salamander (Cryptobranchidae Megalobatrachus japonicus) with special reference to their nerve supply. Annals of Anatomy 174, 235–243. Akita, K., 1992b. An anatomical investigation of the muscles of the pelvic outlet in iguanas (Iguanidae Iguana iguana) and varanus (Varanidade Varanus (dumerillii)) with special reference to their nerve supply. Annals of Anatomy 174, 119–129.

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PART I History, Histology and Development of the Peripheral Nerves

Ange´lica-Almeida, M., Casal, D., Mafra, M., Mascarenhas-Lemos, L., Martins-Ferreira, J., Ferraz-Oliveira, M., et al., 2013. Brachial plexus morphology and vascular supply in the Wistar rat. Acta Me´dica Portuguesa 26, 243–250. Asato, F., Butler, M., Blomberg, H., Gordh, T., 2000. Variation in rat sciatic nerve anatomy: Implications for a rat model of neuropathic pain. Journal of the Peripheral Nervous System 5, 19–21. Ashley, L.M., 1962. Laboratory anatomy of the turtle. W.C. Brown Co., Dubuque, IA. Barone, R., Pavaux, C., Blin, P.C., Cuq, P., 1973. Atlas of rabbit anatomy. Masson & Cie, Paris. Barros, R.A.C., Prada, I.L.S., Silva, Z., Ribeiro, A.R., Silva, D.C.O., 2003. Lumbar plexus formation of the Cebus apella monkey. Brazilian Journal of Veterinary Research and Animal Science 40, 373–381. Baumel, J.J., 1975. Aves nervous system. In: Sisson, S., Grossman, J.D., Getty, R. (Eds.), Sisson and Grossman’s the anatomy of the domestic animals, Vol. 2, 5th ed. W.B. Saunders Co., Philadelphia, pp. 2044–2052. Bensley, B.A., Craigie, E.H., 1938. Practical anatomy of the rabbit: An elementary laboratory text-book in mammalian anatomy, 6th ed. The University of Toronto Press, Toronto. Bertelli, J.A., Taleb, M., Saadi, A., Mira, J.C., Pecot-Dechavassine, M., 1995. The rat plexus brachialis and its terminal branches: An experimental model for the study of peripheral nerve regeration. Microsurgery 16, 77–85. Bertelli, J.A., Mira, J.C., Gilbert, A., Michot, G.A., Legagneux, J., 1992. Anatomical basis of rat brachial plexus reconstruction. Surgical and Radiologic Anatomy 14, 85–86. Bowne, J.G., 1959. Neuroanatomy of the brachial plexus of the dog. PhD Thesis, Iowa State University, Ames. Brooks, W.T., 1883. The brachial plexus of the Macaque monkey and its analogy with that of man. Journal of Anatomy and Physiology 17, 329–332. Carvalho, R.C., Sousa, A.L., Oliveira, S.C.R., Pinto, A.C.B.F., Fontenelle, J. H., Cortopassi, S.R.G., 2011. Morphology and topographic anatomy of the spinal cord of the red-footed tortoise (Geochelone carbonaria Spix, 1824). Pesquisa Veterinaria Brasileira 31, 47–52. Cevik-Demirkan, A., Ozdemir, V., Demirkan, I., Tu¨rkmenoglu, I., 2007. Gross morphological features of plexus brachialis in the chinchilla (Chinchilla lanigera). Journal of the South African Veterinary Association 78, 21–24. Chagas, R.G., Drummond, S.S., Silva, F.O.C., Eurides, D., Alves, E.C.M., Miranda, R.L., 2006. Origem e distribuic¸a˜o do nervo obturato´rio em suı´nos (Sus scrofa domesticus - Linnaeus, 1758) da linhagem AG-1050. Arquivos de Cieˆncias Veterina´rias e Zoologica da UNIPAR 9, 15–20. Champneys, F., 1871. The muscles and nerves of a chimpanzee (Troglodytes niger) and a Cynocephalus anubis. Journal of Anatomy and Physiology 6, 176–211. Chase, R.E., DeGaris, C.F., 1940. The brachial plexus in Macacus rhesus, compared with man. American Journal of Physical Anthropology 27, 223–254. Chiasson, R.B., 1980. Laboratory anatomy of the white rat. W.C. Brown Co., Dubuque, IA Cook, M.J., 1965. The anatomy of the laboratory mouse. Academic Press, New York. Cooper, G., Schiller, A.L., 1975. Anatomy of the guinea pig. Harvard University Press, Cambridge, MA. Crouch, J.E., 1985. Text-atlas of cat anatomy. Lea & Febiger, Philadelphia. Cruz, G.A.M., Adami, M., 2010. Anatomia do plexo braquial de macacobarrigudo (Lagothrix lagothricha). Pesquisa Veterinaria Brasileira 30, 881–886.

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