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The Journal of Bone and Joint Surgery 80:1365-1378 (1998)
© 1998 The Journal of Bone and Joint Surgery, Inc.

Current Concepts Review

Current Concepts Review - Mechanoreceptors in Joint Function*

TOM HOGERVORST, M.D.{dagger}, AMSTERDAM, THE NETHERLANDS and RICHARD A. BRAND, M.D.{ddagger}, IOWA CITY, IOWA

*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.


   Introduction
Top
 Introduction
Anatomical Studies
 Physiological Studies
 Clinical Studies
 Overview
 References
 
Most surgeons and investigators consider ligaments to be passive stabilizers of the joints. However, more than 100 years ago, clinicians and investigators recognized the presence and potential roles of mechanoreceptors in the function of joints52,93,128. Perhaps because of the frequency of injuries of the anterior cruciate ligament, the functional impairment resulting from them, and the issue of whether the anterior cruciate ligament should be removed during total knee replacement, the role of mechanoreceptors in the anterior cruciate ligament recently has attracted considerable attention.

It is important to ascertain the role of mechanoreceptors in the function of intra-articular ligaments in order to determine the future direction of joint reconstruction. Their importance, or lack thereof, will determine, in part, whether efforts should be directed more toward preservation of the receptors or whether the emphasis should remain on purely mechanical and kinematic aspects of joint function.

Joint mechanoreceptors have been most often studied in the knee, with most recent investigations focusing on the anterior cruciate ligament. In exploring the function of mechanoreceptors in the knee, we do not intend to imply that mechanoreceptors in other joints are not important; our review is merely reflecting the literature relating to loss of function of the anterior cruciate ligament due to rupture (injury) or transection (operative treatment) rather than congenital laxity.

The presence of mechanoreceptors in the anterior cruciate ligament41,66,104 has led several authors to suppose that these receptors influence motor function and, conversely, that their loss leads to dysfunction11,40,81. This notion is reinforced by the lack of a clear association between the functional outcome and the amount of passive laxity, not only after non-operative treatment23,38,118,142 of tears of the anterior cruciate ligament but also after reconstruction or repair14,20,70,92,145,160.

Loss of the anterior cruciate ligament alters the kinematics of the knee114 and probably induces a change in the stimulation and the afferent signals or output of the remaining mechanoreceptors—for example, those in the joint capsule55,86. Therefore, the function of the receptors of the anterior cruciate ligament per se must be distinguished from that of the remaining receptors in the knee. In view of the large number31,96 and substantial sensitivity of periarticular receptors59,60,62, an experimental design that explicitly excludes the effects of the remaining receptors is critical for determining the function and importance of the receptors of the anterior cruciate ligament alone.

In this article, evidence that mechanoreceptors may have an effect on neuromuscular function is presented; clinical issues (proprioception, muscle reflexes initiated by the mechanoreceptors of the anterior cruciate ligament, muscle stiffness, quadriceps-force deficits, gait analysis, and electromyographic changes) are discussed; and the relationship between basic (animal) research and the clinical aspects of injuries of the ligament is considered.


   Anatomical Studies
Top
 Introduction
 Anatomical Studies
Physiological Studies
 Clinical Studies
 Overview
 References
 
The terminology that has been used in discussing mechanoreceptors has varied among authors. Freeman and Wyke41 synthesized a number of previous reports and condensed this terminology into four types (Table I). Many but not all authors use their terminology, and so will we, except when it is not appropriate.


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  		TABLE I CLASSIFICATION OF JOINT MECHANORECEPTORS*

 

Relative Scarcity of Mechanoreceptors in the Anterior Cruciate Ligament
Neurotracer studies have indicated that each ligament in a cat contains a total of six to twenty mechanoreceptors104 or, including free nerve-endings, thirteen to fifty-two53 (Table II). There also are very few receptors in humans; monoclonal antibody stains demonstrated a maximum of seventeen mechanoreceptors in the anterior cruciate ligament of a three-year-old child95 (Table III). These numbers decrease with age and disease133,146. Placed in perspective with the innervation of the entire knee joint (as reflected by the total number of afferent nerve fibers), the receptors in the anterior cruciate ligament constitute a small minority (Tables IV and V). Comparable quantitative data are lacking for other ligaments and joints, although mechanoreceptors and free nerve-endings have been found in virtually every joint that has been studied (Tables VI and VII). The scarcity of receptors has been used to argue that they have minor importance. However, there is no a priori reason to believe that small numbers of receptors cannot serve important functions.


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  		TABLE II MECHANORECEPTORS IN THE ANTERIOR CRUCIATE LIGAMENT OF CATS

 

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  		TABLE III MECHANORECEPTORS IN THE ANTERIOR CRUCIATE LIGAMENT OF HUMANS

 

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  		TABLE IV DISTRIBUTION OF FIBER TYPES IN THE NERVES OF THE KNEE JOINT IN CATS*

 

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  		TABLE V CHARACTERISTICS OF TYPES OF FIBERS IN THE NERVES OF THE KNEE JOINT IN CATS*

 

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  		TABLE VI MECHANORECEPTORS IN STRUCTURES OF THE KNEE OTHER THAN THE ANTERIOR CRUCIATE LIGAMENT

 

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  		TABLE VII MECHANORECEPTORS IN OTHER JOINTS

 
Most receptors have been reported to be located in the subsynovial layer and near the insertions of the anterior cruciate ligament (Tables II and III). The synovial tissue that enfolds the anterior cruciate ligament consists of an intimal layer facing the joint cavity and a subsynovial layer, in direct contact with the anterior cruciate ligament, containing neurovascular structures. The posterior articular nerve is the major nerve for the anterior cruciate ligament, although afferent fibers have also been demonstrated in the medial and lateral articular nerves54.

Ruffini Receptors and Free Nerve-Endings
The receptors in the anterior cruciate ligament are primarily Ruffini receptors and free nerve-endings. Ruffini receptors are the most frequently described mechanoreceptors; Pacini receptors are reported less commonly (Tables II and III). Ruffini receptors are thought to function as stretch receptors59,60,74,109, while Pacini receptors seem to be activated mainly by compression24,62. Ruffini receptors have a variable morphology and are classified on the basis of electromicroscopic images65,68. The Ruffini receptors of the subsynovial layer of the anterior cruciate ligament are ovoid in shape and measure approximately fifty by 500 micrometers. They are composed of nerve-endings, endoneural connective tissue, and an incomplete perineural capsule. The endoneural connective tissue consists of collagen fibrils and fibroblasts and is connected to the surrounding tissue through gaps in the perineural capsule66. In ligaments with parallel-oriented fibrils, the perineural capsule is well developed and the Ruffini corpuscles resemble Golgi tendon organs65,68. Pacini receptors have an oval shape; measure approximately 150 by 600 micrometers; and have a thick, lamellated capsule, which consists of fifteen to thirty layers of flat perineural cells. The single afferent fiber, which measures four to eight micrometers, divides inside the capsule into several branches, which then lose their myelin sheath. The nerve terminals are filled with mitochondria and clear vesicles with a diameter of twenty nanometers and with unknown contents66.

While investigators have reported many different classes of receptors in many ligaments (Tables II, III, VI, and VII), these classification systems have been called into question because of several fundamental problems. First, there is controversy about the classification of individual receptors; some authors have suggested that these receptors are not distinct types but rather represent a continuum perhaps related to the adaptation of given receptors to local conditions5,22,65. Second, traditional gold and silver-chloride stains are non-specific and stain vascular and other structures containing collagen and elastin42,130; serial sections are essential for proper interpretation. When such sections have not been obtained, the results of a study are open to question as what appears to be a mechanoreceptor on one or two sections may in fact be a vascular structure32,66,89,102. Third, classification alone does not imply function. Given these and other problems, when inferring function an investigator must interpret studies of types and numbers of receptors with considerable caution.

Free nerve-endings are more numerous than mechanoreceptors and function as nociceptors. They react to inflammation of the joint and pain stimuli, but they also function as high-threshold mechanoreceptors25,72,135-137. In addition, vasoactive neuropeptides such as substance-P and calcitonin gene-related peptide have been reported in 10 per cent (2731 of 27,624) and 33 per cent (373 of 1123) of afferent free nerve-endings69,134. Both of these neuropeptides are found in the cell bodies of the dorsal-root ganglion and their sensory afferent fibers, and both are thought to be involved in the processing of nociceptive information, but they also behave as vasoactive substances50. Thus, afferent free nerve-endings in joints not only transfer information but also serve a local effector function75 by releasing neuropeptides. This local effector function can take the form of diverse possible actions of the free nerve-endings, including vasodilation, an increase in venular permeability, trophic effects, and effects on the immune system75. Free nerve-endings therefore may have a modulatory function in normal tissue homeostasis or in the remodeling of grafts.

Lack of Regeneration of Mechanoreceptors
Mechanoreceptors probably do not regenerate, despite the fact that several reports have suggested that reinnervation with mechanoreceptors occurs after reconstruction of the anterior cruciate ligament13,35. Goertzen et al.51 reported ingrowth of mechanoreceptors into allografts, but that paper has since been withdrawn45. Confirmation of regeneration of mechanoreceptors in conventional histological studies is difficult. Histological examination of the graft material as a control before implantation is needed. Furthermore, the viability and function of the structures that are being reported on ideally should be verified. Verification of the former is possible with use of immunohistochemical methods. In one study in which such methods were used, nerves containing substance-P and calcitonin gene-related peptide were identified in remodeling patellar ligament autogenous grafts in rats8. However, biopsy specimens of patellar ligament autogenous grafts obtained from humans five to thirty-seven months postoperatively showed no neuropeptide immunoreactivity.

A modulatory function of sensory innervation during graft-healing has been hypothesized8. This function may be comparable with the role of neuropeptides in fracture-healing76,116 and myocutaneous flaps87,91. It seems likely that neovascularization is accompanied by ingrowth of neural structures with a neurosecretory paracrine function.

Although some authors have noted the potential for regrowth of mechanoreceptors, only regeneration of free nerve-endings has been documented150,151. Thick, myelinated fibers have never been shown to form new complex endings such as mechanoreceptors. Existing mechanoreceptors can be reinnervated by means of axonal sprouting but only when circumstances are favorable for guiding the axons, as in a successful nerve suture105. Even then, only a small proportion of mechanoreceptors (for example, approximately 20 per cent of Golgi tendon organs) are reinnervated. Moreover, these receptors may function abnormally10,28. Current techniques for reconstruction of the anterior cruciate ligament, such as the drilling of bone tunnels into the femoral origin of the ligament, do not create favorable circumstances for axonal sprouting; in fact, the opposite may be the case.


   Physiological Studies
Top
 Introduction
 Anatomical Studies
 Physiological Studies
Clinical Studies
 Overview
 References
 
In interpreting experimental and clinical work related to the functional loss of mechanoreceptors, two factors must be considered: the direct effect of loss of receptor output, and alterations in the output of the remaining receptors (mainly those of the capsule). The latter consideration is supported by the findings of Khalsa and Grigg86, who studied the responsiveness of capsular mechanoreceptors in cats before and after transection of the anterior cruciate ligament. With use of standardized rotations of the joint, an increase in neural discharge versus joint displacement was seen after transection of the anterior cruciate ligament. This was interpreted as reflecting an increase in capsular stress for a given displacement, which resulted from altered kinematics of the joint.

Unimportant Direct Reflex Effect of Mechanoreceptors on Skeletomotor Neurons
Joint receptors do not have an important direct reflex effect on skeletomotor neurons. Since the 1950s, various authors have attempted to document such an effect of mechanoreceptors of the joint on the muscles surrounding the knee4,26,35,141,147. However, many of these early experiments were confounded by disturbances of muscle or skin receptors. In a well controlled experiment by Grigg et al.61, a weak positive feedback was demonstrated after terminal extension of the knee (quadriceps facilitation and hamstring inhibition). These findings contradict a putative protective reflex. Furthermore, many injuries occur over a time-frame that is shorter (considerably less than ten milliseconds) than that of monosynaptic reflex responses126 (more than twenty milliseconds). Even the weak effect that was noted in the study by Grigg et al. was much less than the effect that was mediated by the afferent-nerve fibers of muscles.

Stimulation of Mechanoreceptors of the Anterior Cruciate Ligament by Hyperextension
Mechanoreceptors of the anterior cruciate ligament are stimulated primarily by hyperextension. Krauspe et al.94, in single-fiber studies, identified a total of twenty-six mechanoreceptors of the cruciate ligament among thirteen animals. No activity was seen with the knee in the resting position of 30 degrees of flexion. All fibers responded to movement, primarily extension, with a marked increase in activity if internal or external rotation was added in extension. Activation also was noted during flexion of the knee.

Lack of Convincing Evidence of a Direct Effect of Mechanoreceptors of the Anterior Cruciate Ligament on the Electromyographic Activity of Muscles Surrounding the Knee
Several methods have been used in an attempt to limit mechanical stimulation to the anterior cruciate ligament. Solomonow et al.144 used traction with a wire loop placed around the anterior cruciate ligament in humans and reported an increase in the electrical activity of the hamstring muscles as measured on electromyograms. Considerable force (130 to 150 newtons) was required as low or moderate force produced no changes. Pope et al.125 repeated this experiment in seven cats with loads as high as 125 newtons (four to five times the body weight of the cats). No effect on the electromyographic activity of the quadriceps or hamstrings was observed, although output in the posterior articular nerve was demonstrated. Normal excitability of reflexes was confirmed with tendon taps, paw pinches, and auditory stimuli. These stimuli easily evoked responses of the quadriceps and hamstring muscles, as seen on electromyograms, in all of the cats. Pope et al. suggested that differences in the method of anesthesia may have induced hyperexcitability in the experiment of Solomonow et al. The use of a loop to pull on the ligament is based on the assumption that no structures other than the intended ligament will be stimulated. Cole et al.27 found this assumption to be questionable. Moreover, increased discharge patterns in the posterior articular nerve occur with as little as thirty micrometers of tibiofemoral motion.

Axial loading with use of traction applied to a block of bone that has been freed along with the tibial insertion of the anterior cruciate ligament seems to be a more appropriate way to isolate mechanical stimulation to the ligament. Miyatsu et al.112 reported electromyographic changes in both the quadriceps and the hamstrings of dogs and cats when traction with forces as high as thirty newtons was applied in this manner. The animals were treated with a precollicular transection (that is, just distal to the thalamus) after removal of the cerebral cortex overlying the mid-portion of the brain and the thalamus. They also had transection of the spinal cord at the mid-thoracic level. It is difficult to interpret these findings as the latency of the changes seems to have been rather long, with the second and largest peak occurring after ten to fifteen seconds. Moreover, the results were not verified with a control experiment after transection of the posterior articular nerve. Therefore, on the basis of the available studies, it must be concluded that an effect of the mechanoreceptors of the anterior cruciate ligament on the electromyographic activity of muscles surrounding the knee has not been convincingly demonstrated.

Influence of Mechanoreceptors of the Anterior Cruciate Ligament on the Output of Muscle Spindles (and Muscle Stiffness) through the Fusimotor System
Johansson et al.81 investigated the hypothesis of Freeman and Wyke40 that ligament receptors influence muscle stiffness through reflex effects involving the fusimotor neurons. Muscle stiffness is defined as the change in length in a muscle-tendon complex for a given change in force. Fusimotor activity was studied indirectly by monitoring the response of 1a muscle-spindle afferent-nerve fibers. These fibers signal the change in the length of the muscle spindles and the speed of this change. An alteration in the response of most of the fibers occurred after traction was applied with use of a wire loop around the anterior cruciate ligament80. Control experiments demonstrated disappearance of the reflex effect in the muscle when traction was applied to the posterior cruciate ligament after section of the posterior articular nerve143.

Therefore, there appears to be convincing evidence that afferent-nerve fibers in the ligament influence muscle-spindle afferent-nerve fibers. However, the functional importance of this phenomenon is far from clear. It may be partly due to the complex input of the fusimotor system79. Johansson et al.81,82 suggested that the fusimotor system, after integrating input from the afferent nerves of skin, muscles, and joints, serves as a final common path for the regulation of muscle stiffness. Although the fusimotor system has a muscle-reflex effect, it acts only in an indirect manner. After muscle spindles have been activated through the fusimotor system, the skeletomotor neurons (alpha motor neurons) are activated through the 1a afferent-nerve fibers. The indirect route and the low conduction velocity of the fusimotor fibers (fifteen to twenty-five meters per second) probably preclude a protective reflex of the joint, as will be discussed later. It should be emphasized, however, that an indirect route does not imply that the receptors are not important in daily function and athletic performance.


   Clinical Studies
Top
 Introduction
 Anatomical Studies
 Physiological Studies
 Clinical Studies
Overview
 References
 
Many patients who have an injury of a lower extremity describe vague symptoms such as unsteadiness (giving-way) of the joint. It seems likely that at least some aspects of these symptoms are related to mechanoreceptors. However, this is difficult to document because of the lack of sufficiently sensitive yet measurable parameters. A tear or removal of the anterior cruciate ligament in humans has been associated with neuromuscular changes such as loss of proprioception, alterations in muscle reflexes initiated by the ligament, alterations in muscle stiffness, quadriceps-force deficits, and changes in gait and electromyographic measurements. However, the findings of many studies12,75,77,78,88,103 are contradictory, partly because of the different criteria for the selection of subjects and the more or less subtle differences in the parameters or methods of measurement. The question remains as to whether these changes are caused by direct loss of mechanoreceptors or by altered stimulation of the remaining receptors, or by a combination of the two.

Proprioception in Patients Who Have a Rupture of the Anterior Cruciate Ligament
Proprioception is the sense of position and movement of the limb and is measured in various ways. Two points should be noted with regard to such measurements. First, no current test of proprioception allows differentiation between the mechanoreceptors of the anterior cruciate ligament and the remaining mechanoreceptors of the capsule and muscles surrounding the knee; thus, these tests generally cannot yield conclusive information about the functional importance of mechanoreceptors of the anterior cruciate ligament. Second, mechanoreceptors of the muscles (muscle-spindle receptors) play an important role in proprioception107. Studies of proprioception after a rupture or reconstruction of the ligament should be interpreted in the broader context of whether mechanoreceptors of the joint or muscles play the primary role in proprioception. Despite extensive reports on this subject during the last two decades, Matthews108 and Proske et al.127 concluded that joint mechanoreceptors (of which ligament mechanoreceptors form only a minority) can signal movement but are unlikely to play a role in position sense. This conclusion is consistent with the absence of mechanoreceptor output in the ligament when the knee is not moving94.

Investigators use two types of tests to measure proprioception: those that ascertain the threshold for detection of passive motion (movement sense) and those that examine the capacity to reposition the limb accurately (position sense). Given the complexity of proprioception, neither test is ideal.

In patients who have a torn anterior cruciate ligament, both increased12,30 and unaltered88,157 thresholds for detection of motion have been reported. Similarly, some authors14,30 have found, with use of a repositioning test, differences in the proprioception of patients who have a torn anterior cruciate ligament, whereas others could not find important differences44,56. More recent studies have suggested possible explanations for these reported differences. Several authors found increased sensitivity of proprioception when the knee was in almost full extension21,44. This observation is consistent with the finding that mechanoreceptors of the capsule and the anterior cruciate ligament respond primarily to terminal extension rather than to movement toward flexion in an almost extended knee58,94. A substantial association between proprioceptive deficits after anterior cruciate rupture and meniscal or chondral lesions also has been documented43. These findings confirm that it is not well known which parameters should be investigated in order to demonstrate a diminished sense of the position or motion of the joint, or both, or what exactly is being tested with current types of examinations. Some of the differences in the results of the mentioned studies probably can be explained by differences in the selection of patients, the method of testing, or the specific devices used for testing.

These limitations also apply to studies of proprioception of the ankle and shoulder. Proprioception after sprains of the ankle has been reported as being both decreased48,98 and unaltered63. Instability of the shoulder has been associated with a decrease in proprioceptive ability, which was restored with operative treatment46,154.

In both the knee and the ankle, proprioceptive ability sometimes improves with use of an elastic bandage or taping79,124,131. This may partly explain the reports of subjective beneficial effects of bracing of the knee despite the fact that biomechanical studies have indicated questionable effects of bracing on strains of the anterior cruciate ligament in tibial translation or rotation18,156.

Lack of Convincing Evidence of a Ligament-Muscle Reflex in Humans
Abbott et al.1, Gardner47, and Palmer123 proposed that motion to the extremes of flexion and extension activates mechanoreceptors of the ligaments, initiating a spinal reflex with contraction of muscles antagonizing the movement (that is, a ligamentomuscular reflex). Such contraction was assumed to take place by direct stimulation of the skeletomotor neurons in order to prevent damage to the ligament and cartilage (a joint protective reflex). In the case of the anterior cruciate ligament, an anterior cruciate ligament-hamstring reflex was proposed64. Such experiments do not allow differentiation between afferent-nerve signals emanating from the anterior cruciate ligament, capsule, and muscles. Furthermore, research in animals has not yielded convincing evidence of an anterior cruciate ligament-muscle reflex, and clinical studies with use of anterior tibial translation to induce a reflex of the hamstrings have yielded conflicting results16,77,155.

Possible Alteration of Muscle Stiffness after a Rupture of the Anterior Cruciate Ligament
In view of the effects of mechanoreceptors on muscle spindles, it is reasonable to presume that such receptors affect muscle stiffness. This concept is based on the model of the muscle-tendon complex as a mass spring system with a damping component that was described by Hill73,103, although such modeling is not unquestioned97. Two studies in which measurements based on this model were used for patients who had a torn anterior cruciate ligament yielded conflicting results78,103.

Loss of Neurosensory Feedback as a Possible Cause of Quadriceps-Force Deficit
Atrophy of the quadriceps is an almost constant finding in patients who have a torn anterior cruciate ligament49,83,100,117,160. Several authors found a decrease in extensor torque that was larger than would be expected on the basis of the decrease in the volume of the quadriceps as measured with computed tomography37,39,83,99,100. The hamstring muscles do not have a comparable force deficit. Specific physiotherapy can only partially correct the deficit142. The difference in torque has been reported to persist after reconstruction of the anterior cruciate ligament with use of autogenous grafts or allografts from the patellar ligament142,159 or with use of semi-tendinosus grafts92,132.

Under static conditions, the integrated electromyogram reflects the number of activated muscle fibers and their frequency of discharge. Several researchers found a lower summed electrical activity (integrated electromyogram) in the affected limb after both operative treatment (reconstruction with use of a bone-patellar ligament-bone autogenous graft)29,39 and non-operative treatment36,37,39 in patients who had a torn anterior cruciate ligament. (An integrated electromyogram is obtained from the summed electrical activity of a muscle in a given period of time. This can be calculated by integrating the surface under the curve of the electromyogram for the time-period.) However, the electrical efficiency of the muscle (the ratio of the integrated electromyogram to work) is unchanged in the affected limb29,36,39. These findings led Elmqvist et al.36 to propose that the deficit in strength is the result of decreased stimulation of the quadriceps muscle in the central nervous system. A decrease in the activation of the quadriceps muscle at a spinal or higher level could be a consequence of an alteration in the afferent signals after a tear of the anterior cruciate ligament.

Gait Analysis
Gait analysis shows functional adaptations in a high proportion of patients who have a tear of the anterior cruciate ligament. Such analysis of patients who have a chronic tear of the anterior cruciate ligament has shown a decrease in the flexion moment of the knee in the range of 0 to 40 degrees of flexion7,17. When the normal limb moves into the mid-stance phase, gravity and inertia generate a moment that tends to flex the knee. This external flexion moment is balanced by the quadriceps muscles (internal extension moment); therefore, a decrease in the flexion moment suggests a decrease in the quadriceps muscle moment6. Such a decrease was seen in both limbs of patients who had only one knee with a torn anterior cruciate ligament17. Andriacchi6 termed this finding the quadriceps-avoidance gait. Not all patients who have a torn anterior cruciate ligament have such a gait. Its prevalence is partly related to the time since the injury19. In activities that involve knee-flexion angles of less than 30 degrees (that is, those involving normal gait), the quadriceps-avoidance gait is most effective in preventing anterior tibial translation6,110,111. In activities that involve knee-flexion angles of 40 degrees or more (for example, jumping or sharp changes in running direction), increased contraction of the hamstrings is effective in preventing anterior tibial translation111,113,122,129. Both mechanisms precede the event that they are meant to antagonize. This is possible only if the joint-capsule receptors that signal the event transfer information to higher centers, followed by modification of motor programs (that is, a learning process). Conversely, reflex-like mechanisms can be excluded on the basis of the time-frames that are involved126. It is assumed, although not yet proved, that these functional adaptations are beneficial to patients who have a torn anterior cruciate ligament.

Functional Adaptations after a Tear of the Anterior Cruciate Ligament to Prevent Damage to Secondary Restraints and to Stabilize the Knee during Stressful Activities
The prevalence of secondary meniscal lesions and associated degenerative joint disease in patients who have a torn anterior cruciate ligament115 seems to confirm the increased stress on the menisci in a knee with a torn anterior cruciate ligament111. A decreased quadriceps moment in patients who have a quadriceps-avoidance gait thus may be a protective mechanism for the secondary restraints. The development of a quadriceps-avoidance gait may depend on chronic stretching of the joint capsule, but it probably also depends on other factors, such as the ability of motor programs (neural networks that govern specific, often repeated motions) to adapt to a changing stimulus. Additional support for this concept is found in studies of dogs in which the anterior cruciate ligament was transected. Kinematic studies demonstrated increased anterior tibial translation throughout the stance phase after transection of the anterior cruciate ligament in dogs. The dogs compensated by decreasing the limb load and increasing flexion of the knee throughout the gait cycle, but they were unable to prevent subluxation of the joint in the stance phase90. (Because the dogs were studied six weeks after transection of the anterior cruciate ligament, it is not known whether functional adaptations would have developed.) Transection of the anterior cruciate ligament leads to slight degenerative changes in the cartilage, but additional deafferentation of the knee joint produces severe degenerative changes121,153. This suggests that sensory input from the joint may play a role in adapting movement strategies so that potentially harmful positions and loads are prevented, thus decreasing the rate at which an unstable joint degenerates.


   Overview
Top
 Introduction
 Anatomical Studies
 Physiological Studies
 Clinical Studies
 Overview
References
 
It can be presumed that injuries to ligaments have two neurosensory effects: a loss of signaling from the mechanoreceptors in the torn ligament and a gain in signaling from the mechanoreceptors in the periarticular tissues as a result of instability. The fact that the functional outcome of a torn anterior cruciate ligament is not directly associated with the amount of laxity may be related to the variable adaptation of patients to loss or gain of signals. We propose the following.

1. Mechanoreceptors in ligaments are part of a complex of several receptor populations providing input that influences muscle stiffness. The fact that several other (potentially redundant) receptor populations have input into this system can be used to argue that the relatively few receptors in most ligaments are of minor importance in this context and that the loss of receptor input may be compensated for by the remaining receptors. However, the precise role of various receptors may vary from individual to individual, so loss of mechanoreceptors or failure to adapt by means of redundant sources may be more critical in some patients than in others.

2. Specific considerations for the quadriceps may be justified. The anterior cruciate ligament and the quadriceps are mechanical antagonists. Extension of the knee generates strain in the anterior cruciate ligament, activating mechanoreceptors in the ligament. Contraction of the quadriceps muscle further increases anterior-cruciate-ligament strain in the extended knee. The anterior cruciate ligament is the only structure that specifically antagonizes the anterior tibial translation generated by the quadriceps muscle; thus, its mechanoreceptors may be the only ones that sensitively and effectively signal anterior tibial translation. It therefore seems reasonable to assume that the output of the anterior-cruciate-ligament mechanoreceptors has a specific influence on the function of the quadriceps. The fact that only a few mechanoreceptors are present need not signify that the receptors are unimportant as they may be the only receptors that are involved in this function. On the basis of the quadriceps-force deficit after a tear of the anterior cruciate ligament, it can be hypothesized that this proposed function may facilitate activation of the quadriceps when the anterior-cruciate-ligament strain is within certain limits. Assuming that a direct reflex influence is unlikely, it might be proposed that the output of the anterior-cruciate-ligament mechanoreceptors has a modulating effect on motor programs in which the quadriceps muscle plays an important role. Traditional views have been based on the concept of direct reflexes, but it may be more realistic to incorporate the concept of a history of loading instead of a single loading event into any hypothesis regarding the function of such receptors.

3. On the basis of the neuropeptide expression of afferent free nerve-endings, it appears that these fibers may play a role, in conjunction with the efferent fibers, in maintaining homeostasis of the ligament (or a remodeled graft); that is, they may play a role not only in the regulation of blood flow but also in the turnover of collagenous tissues. Whether a mechanoreceptor-mediated response to the loading history of the ligament also contributes to this is entirely speculative.

Potentially testable hypotheses could be formulated for all three proposed functions. Most of the necessary experiments will have to be based on selective blockade of the afferent-nerve fibers of the anterior cruciate ligament in combination with a sensitive outcome measure. It seems likely that the mechanoreceptors of ligaments associated with other joints will be comparable with those of the anterior cruciate ligament, with regard to the first and third functions. What seems obvious is the presence of mechanoreceptors and their clear roles in functions that are subtle or difficult to measure. However, such subtlety cannot be taken to mean that mechanoreceptors do not have important implications for function or performance. As more sensitive measures are developed, it will be possible to study the true roles of these receptors and to determine what must be done to facilitate recovery after their loss.


   Footnotes
 
{dagger}Department of Orthopaedic Surgery, OLVG Hospital, P.O. Box 95500, 1091 HM Amsterdam, The Netherlands.

{ddagger}Department of Orthopaedic Surgery, University of Iowa Hospitals and Clinics, 2430 Steindler Building, Iowa City, Iowa 52242-1008.


   References
Top
 Introduction
 Anatomical Studies
 Physiological Studies
 Clinical Studies
 Overview
 References
 

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