INTRODUCTION
In the middle of the 19th century, Rüdinger was the first to describe the presence of innervation in ligaments. In his macroscopic study on the neural anatomy of human joints, nerves were described as coursing through ligaments. Almost one century would pass, however, before the detailed neural topography of ligaments was mapped by Gardner, Kellgren and Samuel, Skoglund, and, later, Freeman and Wyke. Using various staining techniques and light microscopy, the first detailed accounts of nerve endings were described. These endings were subsequently labeled as mechanoreceptors , indicating a specific neural structure sensitive to the mechanical forces acting on the ligament. Since then, a great number of articles have been published on the innervation of ligaments in cats, dogs, and humans.
The first study on the presence of mechanoreceptors in the human wrist joint was reported by Petrie and colleagues in 1997. Using gold chloride staining technique, same as their pioneering predecessors, the researchers identified mechanoreceptors in three volar wrist ligaments. Since their report, the advance of immunohistochemical techniques and digital microscopy (light- and confocal) has allowed a more detailed description of nerve endings in the wrist ligaments. The aim of this chapter is to introduce the reader to the neural structures found in the wrist and distal radioulnar ligaments, the varying distribution pattern in the carpus and the distal radioulnar joint (DRUJ), and the implications this may have on wrist sensorimotor function.
TYPES OF INNERVATION
Classification
The classification of nerve endings in ligaments has been a subject of much debate. While nerve endings are readily identified in the microscope, the concept of classifying them as encapsulated, dendritic, or free nerve endings is quite a challenge to the examiner. The advancement of immunohistochemical techniques has allowed a more detailed analysis of these structures than the archaic silver and gold staining techniques. By using immunohistochemical markers targeted toward specific components of nerves and nerve endings, along with thin serial sections of specimens (5 to 10 μm), a receptor image can be built up. For instance, the use of protein gene product (PGP) 9.5 or tyrosine kinase receptor B (trkB) can identify the axon of the nerve and the core of the receptor; S100 targets Schwann cells, whereas p75 illuminates the perineurial area and the capsule of the receptors ( Fig. 2-1 ). With the addition of confocal microscopy and digital imagery, the complexity of receptor structures has become even more evident ( Fig. 2-2 ).
While the advent of digital techniques may, in the future, lead to a new definition of nerve endings in ligaments, the most common classification system still in use today is that proposed by Freeman and Wyke in 1967 ( Table 2-1 ). The major drawback with this system is its nominative and eponymic, rather than descriptive, method of classification.
| Type | Eponym/Name (descriptive) | Characteristic | Neurophysiologic Trait | Role in Joint Function | Immunoreactivity (IR) Patterns |
|---|---|---|---|---|---|
| I | Ruffini (dendritic) | Coil-shaped, partial encapsulation, dentritic nerve endings with bulbous terminals, 50–100 μm |
|
|
|
| II | Pacini (lamellated) | Rounded, ovular corpuscle; thick lamellar capsule, 20–50 μm |
| Joint acceleration/deceleration |
|
| III | Golgi-like (grouped dendritic) | Large, spherical; partial encapsulation; groups of dendritic endings, >150 μm |
| Extreme ranges of joint motion |
|
| IV | Free nerve endings | Varicose appearance, often close to arterioles; groups or single fibers |
| Noxious, nociceptive, inflammatory |
|
| V | Unclassifiable | Variable size, appearance, and degree of encapsulation |
| Unknown |
|
Types of Nerve Endings
Ruffini Ending
In the late 19th century, Angelo Ruffini, an Italian histologist, identified the Ruffini ending as a partially encapsulated receptor, consisting of an afferent axon ending in a dendritic coil-shaped corpuscle (see Fig. 2-2 ). Each of the ramifications in the corpuscle has a bulbous nerve ending, lodged between the fibrils of collagen in the ligament. This design makes the Ruffini ending ideal for sensing changes in tension and direction in the collagen fibers. It is the predominant receptor type found in the wrist ligaments and functions as a slowly adapting, low-threshold receptor, constantly firing at a low rate. It is believed to be important in the constant monitoring of static joint position, as well as changes in amplitude and velocity of joint rotations.
Pacini Corpuscle
In 1831, Italian anatomist Filippo Pacini discovered the corpuscle that carries his name, the Pacini corpuscle. Although the eponym is primarily used for this receptor, it is at times referred to as a lamellated sensory corpuscle, indicating the thick capsule that characterizes this nerve ending. Histologically, a Pacini corpuscle consists of a central axon (see Fig. 2-1 A and B) surrounded by layers of perineurial lamellae, which create a distinguishing capsule (see Fig. 2-1 C). In the ligament, this receptor is quite small with a diameter of 20 to 50 μm. The Pacini corpuscle in the skin and the palm of the hand is highly sensitive to vibrations and skin indentations, but its function in the ligament is as a low-threshold, rapidly adapting receptor active only in joint acceleration and deceleration. It is considered a pure dynamic mechanoreceptor and, though present in the wrist ligaments, is rare compared with the Ruffini ending.
‘‘Golgi Tendon Organ”
Named after the 1906 Nobel laureate in physiology or medicine, Camillo Golgi, the expression “Golgi tendon organ” is, in fact, a misnomer in terms of ligament innervation and should be reserved for the specialized nerve ending found in the myotendinous junction. The nerve ending intended in the ligament is a type of spray ending, belonging to the same family as the Ruffini ending. It is characterized by a large (more than 150 μm in diameter) partially encapsulated receptor with groups of arborizing nerve endings at its core ( Fig. 2-3 ). More suitable names for this receptor include large Ruffini ending, grouped dendritic nerve ending, or, if need be, Golgi-like. It is rarely found in the wrist ligaments, but more commonly found in larger ligaments such as the anterior and posterior cruciate ligaments. It is a slowly adapting, high-threshold receptor, which is believed to be active only at the extreme ranges of joint motion.
Free Nerve Endings
The free nerve ending denotes a terminal sensory axon without perineurial layers or concomitant corpuscles. These bare endings are of A-delta or C fiber types and are highly sensitive to a number of chemical agents, such as histamine and prostaglandin. As such, they are believed to be important in noxious, inflammatory, and nociceptive responses in the joint.
Unclassifiable Corpuscles
A large number of corpuscles observed in ligaments are classifiable neither as Pacini nor Ruffini. These are receptors of varying sizes and appearances, and their exact role in joint proprioception remains unknown.
DISTRIBUTION OF NERVE ENDINGS IN THE WRIST
Innervation of the Wrist Joint
The dorsal wrist capsule and the dorsal wrist ligaments are primarily innervated by the terminal branch of the posterior interosseous nerve (PIN), the dorsal interosseous nerve (DIN), which arborizes in the fourth extensor compartment and distributes branches to the majority of the dorsum of the wrist. In addition, the dorsal sensory branch of the radial nerve and the dorsal sensory branch of the ulnar nerve innervate the dorsoradial and dorsoulnar aspects of the wrist, respectively ( Fig. 2-4 ).
While the innervation of the dorsal wrist is quite constant and predictable, the innervation pattern of the volar wrist is more diverse, and several dissection studies have been published on the anatomic variances as related to surgical denervation of the wrist. In general, the volar wrist capsule and the radioscapholunate (RSL) ligament receive branches from the anterior interosseous nerve (AIN), whereas the volar carpal ligaments appear to receive their innervation from the lateral antebrachial cutaneous nerve, the volar cutaneous branch of the median nerve, the deep branches from the ulnar nerve, and the endings from the anterior interosseous nerve.
Innervation of the Distal Radioulnar Joint
The innervation to the distal radioulnar joint and triangular fibrocartilage complex (TFCC) appears to be threefold, with the dorsal region primarily innervated by the dorsal interosseous nerve, the ulnar region primarily by the dorsal sensory branch of the ulnar nerve, and the volar region by branches from the ulnar nerve. While dissection studies have shown anterior interosseous nerve branches in the vicinity of the palmar distal radioulnar joint capsule, detailed microscopic studies have not been able to show anterior interosseous nerve afferents in the distal radioulnar ligaments. The same holds true for the medial antebrachial cutaneous nerve, which has an extra-articular course in the distal radioulnar joint but lacks intra-articular contributions.
Innervation Pattern in the Ligaments
In a recent publication on the innervation of 14 important wrist ligaments, we found a distinct pattern with regard to ligaments that were innervated compared with those that had little or no innervation. In the former, mechanoreceptors and nerve fascicles were consistently found in the loose connective tissue of the superficial region of the ligaments, the so-called epifascicular region. In this pliant tissue, the nerves were found to course through the ligament, often in the vicinity of blood vessels. The density of innervation was greatest close to the ligament insertions into bone, as well as throughout the epifascicular region. This trait of distribution has subsequently been confirmed in the dorsal radiocarpal ligament, as well as in the TFCC.
On the other hand, ligaments with little or no innervation were primarily composed of thick parallel bundles of collagen in the core, or fascicular region , of the ligament. Hence, ligaments that are richly innervated have a large epifascicular region compared with ligaments with sparse innervation that are predominantly compact collagen structures, designed for mechanical stability and resilience ( Fig. 2-5 ). There would thus seem to be a correlation between the anatomic design and proprioceptive or mechanical function, rendering the wrist ligaments a complexity hitherto unknown.
Related posts:
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Arthroplasty of the Distal Radioulnar Joint
External Fixation of Distal Radius Fractures
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Bone Tumors of the Hand and Wrist
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