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Article: Dee R. Structure and function of hip joint innervation (1969). The author discusses the nervous system of the ligamentum capitis femoris (LCF) and its role in hip biomechanics. The text in Russian is available at the following link: 1969DeeR.


STRUCTURE AND FUNCTION OF HIP JOINT INNERVATION

Arnott Demonstration delivered at the Royal College of Surgeons of England on 4th February 1969

by Roger Dee, M.A., F.R.C.S.

Neurologcal Laboratory, Royal College of Surgeons of England, and

Department of Orthopaedic Surgery, Middlesex Hospital, London

 

In 1885 JAMES ARNOTT, surgeon to the Middlesex Hospital and one of the founders of its Medical School, endowed a series of lectures to be given at the Royal College of Surgeons on the contents of its Museum. Two years previously, at the same hospital, Arnott's colleague Bland-Sutton had demonstrated the interest of Middlesex surgeons in hip joint function with his famous paper on the ligamentum capitis femoris; and in the Orthopaedic Department at the Middlesex Hospital to-day, one of our chief clinical problems continues to be disordered function in this joint. This is a problem with which Arnott must surely have been familiar, and one with which I wish to deal in this lecture.

Multi-disciplinary approaches to orthopaedic problems are currently breaking new ground and yielding fundamental information on the structure and function of joints; and, in pursuing such an approach, recent studies of the subject of articular neurology in the Neurological Laboratory of the Royal College of Surgeons of England (under the supervision of Dr. Barry Wyke) have embraced the temporo-mandibular, laryngeal, spinal, knee and ankle joints (Freeman and Wyke, 1966, 1967a, 1967b; Greenfield and Wyke, 1966; Kirchner and Wyke, 1965; Wyke, 1967). These studies have underlined the hitherto underrated importance of the specific mechanoreceptors located in all the articular tissues, which have been shown to exert powerful reflex effects on the static and dynamic regulation of muscle tone, as well as contributing to perceptual awareness of joint position and movement.

In this demonstration I am reporting some of the findings in our investigation of the neurology of the hip joint that is being pursued in collaboration with Dr. Wyke and Dr. Barrie Tait of the Rheumatism Research Centre, the University of Manchester, and with the support of the Camilla Samuel Fund. The first part of this investigation involved a combined anatomical and histological study of the innervation of 63 hip joints in 37 mature cats, supplemented by a histological study of fresh articular tissues removed at operation from five adult human hip joints. 

THE INNERVATION OF THE HIP JOINT 

The extrinsic innervation of the hip joint was studied by three different procedures:

1. In fresh, unfixed cadavers, 41 hip joints were dissected (using a binocular dissecting microscope when necessary) to identify the articular branches of the peripheral nerves in the pelvis and thigh. These branches were individually traced into the various regions of the hip joint capsule and into the ligamentum capitis femoris. In some instances dissection of intramuscular nerve branches was performed after preliminary maceration of the tissues in warm 1 per cent acetic acid.

2. Surgical dissections of each of the articular branches of the peripheral nerves in the pelvis and thigh were performed on 22 occasions with a binocular operating microscope in anaesthetized animals, preparatory to their electrical stimulation-the results of which I will describe later.

3. Articular nerves freshly resected from anaesthetized cats were examined histologically with a modified paraffin silver technique to determine their fibre composition. Nerve fibre counts and diameter measurements were made on photomicrographs enlarged one thousand times.

These macro- and micro-dissection studies show that the hip joint, like other limb joints, is densely innervated by primary and accessory articular nerves-the former being direct articular branches of adjacent peripheral nerve trunks, and the latter articular twigs arising from nerves within the substance of muscles related to the joint. 

Primary articular nerves

The three primary articular nerves may be classified in terms of their topographical relationship to the hip joint, and the sector of the joint capsule that they innervate. They are sufficiently constant to permit routine identification. They have been designated as the medial articular nerve, the nerve to the ligamentum capitis femoris, and the posterior articular nerve.

The posterior articular nerves (Fig. la) consist of a varying number of short (5-6 mm long) articular branches of the nerve to the quadratus femoris muscle, and represent the most prolific supply to the hip joint. They arise at intervals on the lateral aspect of the main nerve trunk proximal to its termination in the belly of the quadratus femoris muscle. They pass laterally on the surface of the ischium, beneath the obturator internus tendon and the gemelli muscles, to enter the posterior capsule of the joint (accompanied by fine articular blood vessels) through the full extent of its acetabular attachment. The middle and superior branches curve upwards along the acetabular rim to supply the posterior joint capsule as far superiorly as the level of the inferior border of the gluteus minimus muscle, whilst the inferior branches run directly along the upper border of the obturator externus to be distributed to the postero-inferior regions of the joint capsule and the ischio-femoral ligament.

The medial articular nerve (Fig. 1b) usually arises as a single articular branch from the anterior division of the obturator nerve. The anterior division separates within the obturator canal into medial and lateral branches that leave the obturator foramen above the superior border of the obturator externus muscle; and the first muscular twig of the lateral branch of the anterior division gives off the medial articular nerve before terminating in the pectineus and adductor muscles. The articular nerve then divides into two terminal filaments that are distributed to the antero-medial and inferior aspects of the joint capsule-that is, to the region medial to the plane of the ilio-psoas muscle. Occasionally the muscular branch giving rise to the medial articular nerve comes off the main trunk of the obturator nerve within the obturator canal. On no occasion in our material did the medial articular nerve arise from the posterior division of the obturator nerve or any of its branches.

The nerve to the ligamentum capitis femoris is consistently provided as an independent articular nerve that arises from the muscular branch of the posterior division of the obturator nerve that supplies the obturator externus muscle. This muscular branch usually arises as the first laterally directed branch of the posterior division of the obturator nerve at the external orifice of the obturator foramen, but it may arise within the obturator canal. It passes laterally between the deep surface of the obturator externus muscle (in which it eventually terminates) and the ventral surface of the ischium. The articular branch is given off from it about 3-4 mm from the obturator foramen (Fig. 2a). The articular nerve, which is about 2-3 mm long, enters the acetabular notch bound up with articular blood vessels, and breaks up into filaments that ramify longitudinally along the surface of the ligamentum capitis femoris to which it is exclusively distributed, apart from a few twigs given off to the acetabular fat pad in the cotyloid notch. The hip thus resembles the knee joint (Freeman and Wyke, 1967b) in that its intra-articular ligament the ligamentum capitis femoris is provided with an independent articular nerve, as are the cruciate ligaments within the knee joint. 

Accessory articular nerves 

The hip joint is more like the ankle (Freeman and Wyke, 1967c) than the knee in respect of the fact that only very small proportion of its innervation is provided through accessory articular nerves. On only two occasions was it possible to demonstrate an accessory articular nerve posteriorly. When present, this accessory articular nerve was provided as a branch of the muscular nerve given off by the superior gluteal nerve to supply the gluteus quartus muscle. No other accessory articular nerves were found to arise from the muscular branches of the superior gluteal nerve to the gluteus medius, gluteus minimus and tensor fasciae muscles, in spite of repeated dissections of macerated specimens. Likewise, the inferior gluteal and pudendal nerves, and the nerves to the superior gemellus and piriformis muscles, were not found to contribute articular branches to the hip joint in any specimen examined. The obturator nerve did not provide any accessory articular nerves in our material, which is perhaps not surprising since it is the source of two relatively constant primary articular nerves to the hip joint. By contrast with the obturator nerve, the femoral nerve is responsible for providing most of the accessory innervation to the hip joint, by accessory articular nerves which arise from its muscular branches. No primary articular nerves arise from the femoral nerve trunk-which confirms the findings of other workers on human and animal material. We agree also with previous workers that the only constant femoral innervation to the hip joint is provided by accessory articular branches from the nerve to the pectineus muscle.

The nerve to the pectineus muscle (Fig. 2b) arises within the femoral sheath from the first lateral branch of the saphenous nerve and pierces the postero-medial edge of the femoral sheath. A varying number of articular twigs are given off from the nerve near its termination, and reach the antero-medial and inferior aspects of the joint capsule either by passing through the lateral edge of the psoas muscle or the medial edge of the pectineus muscle, or by running to the joint in the areolar tissue between these two muscles.

Accessory articular nerves were infrequently provided from some of the branches of the femoral nerve supply to the quadriceps musculature, especially those branches to the rectus femoris and the vastus medialis muscles which arise distally from the main branches of the femoral nerve and run a recurrent course to the proximal ends of these muscles. No accessory articular nerves were found to arise from the muscular branches of the femoral nerve supplying the vastus intermedius, lateralis or sartorius muscles.

In just over one-quarter of his human material, Polacek (1963) described an accessory femoral nerve arising directly from the second and third roots of the lumbar plexus that supplies the pectineus muscle and gives off an articular branch to the hip joint. Such a nerve was not present in our cat material, but a constant intramuscular branch of the femoral nerve arose from the main trunk within the substance of the psoas muscle (some 4 cm proximal to the joint) and pursued a similar course to supply the psoas and rectus femoris muscles, and often gave off a branch to the antero-lateral joint capsule. 

Structure of articular nerves 

Articular nerves, as they penetrate into the capsular tissues of the hip joint in both cat and man, contain a mixture of myelinated and unmyelinated fibres, the former having a diameter of up to 1 3p, with a few fibres as large as 17p. All the myelinated fibres larger than 5-6p in diameter terminate in three types of end-organs of differing size and morphology, whilst the smaller myelinated and most of the unmyelinated fibres terminate in nerve plexuses ramifying through the fibrous capsule and fat pads of the joint or as free nerve endings with the joint ligaments. The remainder of the unmyelinated fibres terminate in the walls of the articular blood vessels distributed throughout the fibrous joint capsule and the subsynovial fibro-adipose tissue.

Articular nerve endings 

Fresh tissues removed from the hip joints of ten of the anaesthetized animals were treated with four different histological methods, involving specially modified gold chloride, methylene blue, frozen silver and paraffin silver techniques, and examined microscopically for nerve fibres and endings. Serial sections from each type of tissue were studied (including the individual quadrants of the fibrous joint capsule, and the ligamentum capitis femoris) to estimate the regional population density of the nerve endings. Measurements of the dimensions of end-organs, and of the caliber of the nerve fibres within the articular tissues, were made on enlarged photomicrographs. Similar studies were made of fresh tissues from various regions of five human hip joints, the material being obtained in the course of surgical operations on the hip and processed immediately. On the basis of these studies we have classified the nerve endings in the articular tissues into four varieties (see Freeman and Wyke, 1967b; Wyke, 1967) that are morphologically and functionally distinct. 

Type I endings (Fig. 3a) are more densely distributed in the hip joint than in the more peripheral knee and ankle joints. They are small, globular, encapsulated corpuscles located mainly in the superficial layers of the fibrous capsule in three-dimensional clusters. In the hip they are sparse in the superior parts of the joint capsule, but are profuse in the inferior capsular regions in front of and behind the joint. These corpuscles behave collectively as a low threshold, slowly adapting mechanoreceptor system responding to changing patterns of stress in the joint capsule. Their fluctuating discharges reflexly affect muscle tone, both at rest and during movement, and they are also the principal contributors to perceptual awareness of static joint position and joint movement. 

The Type II endings (Fig. 3b) are seen infrequently in the hip compared with the more peripheral limb joints, and are distributed in clusters mainly in the deeper layers of the fibrous capsule. Each Type II end-organ is an elongated corpuscle with a thick connective tissue capsule, within which a terminal unmyelinated axon is surrounded by a layer of cells containing granular cytoplasm. The Type II corpuscles function as low threshold, rapidly adapting mechanoreceptors. They are inactive when the joint is at rest, but at the onset of movement they respond to the altered stress in the joint capsule with a brief burst of impulses that lasts for only half a second or less, and which provokes transient reflex adjustments in muscle tone. Unlike the Type I endings, the Type II receptors appear not to contribute to perceptual awareness of joint position, being purely reflexogenic. 

As in other joints, the Type III endings (Fig. 3c) are confined to the joint ligaments. In the hip they are found on the surfaces of the major extrinsic ligaments and of the ligamentum capitis femoris. Morphologically the Type III end-organs are large, fusiform, thinly encapsulated corpuscles supplied by a large myelinated nerve fibre that breaks up within the corpuscle into many unmyelinated club-like filaments. These end-organs behave as high threshold, slowly adapting mechanoreceptors. They are inactive at rest and remain so during moderate degrees of joint displacement; but they reflexly inhibit the tone of prime movers when they are activated at the extremes of joint movement. 

The Type IV articular receptor system (Fig. 3d) consists of unencapsulated nerve endings arranged as plexuses in the joint capsule, and as free endings in the ligaments, that function as the articular pain receptor system. Figure 3 (d) shows such a lattice-like receptor system in the fibrous capsule of the hip joint, within which it is most dense posteriorly and inferiorly. A comparable pain receptor system (but of free endings) is present in the ligamentum capitis femoris. No nerve endings of any description are present in the synovial tissue of the hip, as is the case with all other synovial joints (Wyke, 1967). 

ARTICULAR REFLEXES FROM THE HIP JOINT 

I should now like to offer some experimental evidence of the fact that the copious innervation of the hip joint that I have outlined exerts significant influences on the reflex regulation of the tone of the muscles related to the joint. 

Direct stimulation of articular nerves 

In the first series of experiments, simultaneous bilateral electromyography of all the muscles operating over both hip joints was performed during direct electrical stimulation of the primary articular nerves with graded stimulus parameters in 14 lightly anaesthetized cats. The animal's body and limbs were immobilized by fixation to a rigid scaffold attached to the operating table. The degree of anaesthesia was controlled from continuous monitoring of the animal's pulmonary ventilation rate.

Powerful ipsilateral and contralateral reflex effects were provoked by stimulation of the articular nerves to the hip joint. As Figure 4 illustrates, moderately intense stimulation of the medial articular nerve supplying the antero-medial joint capsule results in powerful bilateral facilitation of the adductor musculature, more marked contralaterally, that is accompanied by inhibition of motor unit activity in both biceps femoris muscles. At the same time, there is weaker facilitation of the ipsilateral rectus femoris and gluteus medius muscles. As the threshold of the articular afferent fibres is inversely proportional to their diameters, the responses depicted here represent the reflex effects of excitation of the larger diameter mechanoreceptor afferents in the nerve. The responses were abolished in this, and all other experiments, by section of the nerve proximal to the stimulating electrodes.

Additional excitation of the smaller diameter afferent fibres contained in the same articular nerve by more intense stimulation changes the pattern of the reflex response. The effects on the biceps femoris musculature are unaltered; but there is a reduction in reflex facilitation of the adductors and abductors of the hip that is accompanied by increased facilitation of the ipsilateral rectus femoris muscle and inhibition of the contralateral rectus. The pattern of response obtained was very variable, and altered readily with relatively small changes in stimulation voltage as a different nerve fibre spectrum responded. Sometimes a different pattern was elicited by the same stimulus parameters at a different period of the experiment when the animal was at a slightly different stage of anaesthesia. With low voltage stimulation, inhibitory responses were seen which were transient and not as powerful as the facilitatory effects seen at higher voltage. These responses are due to stimulation of the very large diameter fibres originating in Type III receptors. It is noteworthy that facilitation of the adductor group was an effect common to all our experiments on this nerve, and that this facilitation was powerful and often bilateral.

The existence of regional specificity of the articular reflex responses is illustrated in Figure 5, which shows the effect of moderate stimulation of a posterior articular nerve distributed to the postero-superior joint capsule. As with previous stimulation of the anteriorly distributed nerve there is still bilateral adductor facilitation, but now it is more marked ipsilaterally than contralaterally. The most marked difference, however, is the appearance of ipsilateral biceps facilitation, though the contralateral biceps muscle is still weakly inhibited. More intense stimulation of the same posterior articular nerve augments the degree of inhibition of the contralateral biceps femoris muscle, and also converts the previous facilitation of the contralateral adductor musculature to inhibition. The response to stimulation again varied with the stage of anaesthesia and with the stimulus parameters.

By contrast, stimulation of an inferiorly distributed posterior articular nerve, which innervates the ischio-femnoral ligament and its Type III receptor population, results (Fig. 6) in profound, prolonged inhibitory responses affecting almost all the musculature sampled. What is of interest is that this is another example of regional specificity, and that this pattern was quickly established at low voltage stimulation and remained relatively unaltered in spite of changes in the stimulus parameters. This typical inhibitory pattern was also demonstrable with the identical nerve of the contralateral hip in the same animal, and is remarkably constant from animal to animal.

Direct electrical stimulation of the extra-acetabular trunk of the nerve to the ligamentum capitis femoris on one side of the body led to reflex changes in the tone of the muscles operating over both hip joints that again varied in magnitude according to the stimulus parameters and the stage of general anaesthesia, and which were totally abolished by section of the nerve proximal to the stimulating electrodes. With stimulus intensities just above threshold (Fig. 7) the most marked effect is powerful inhibition of the ipsilateral adductor musculature that is accompanied by brief facilitatory bursts in both biceps muscles and the ipsilateral rectus. The inhibition of the adductor musculature continues for several seconds longer than the duration of the stimulus, and the facilitation of the other muscles is eventually replaced by inhibition.

With higher stimulus intensities (Fig. 8), profound inhibition bilaterally of all the muscles of the hip joint is produced. This inhibitory response resembles the response seen previously with the inferiorly distributed posterior articular nerves that innervate the ischio-femoral ligament, and is a reflection of the fact that these nerves contain a high proportion of very large diameter fibres that innervate the Type III corpuscles in the acetabular and femoral extremities of the ligament. When the glutei are sampled during stimulation of the nerve to the ligamentum capitis femoris, ipsilateral gluteal facilitation often accompanies the adductor inhibition.

These findings suggest to us that a major function of the ligamentum capitis femoris might be reflexogenic, and further support for this hypothesis was provided in our next series of experiments. 

Passive movement stimulation of articular mechanoreceptors 

Application of graded mechanical stresses in various directions to the hip joint capsule, and to the ligamentum capitis femoris, was performed by manipulation of the isolated upper end of one femur during simultaneous bilateral electromyography of the same muscles as before in a further 11 anaesthetized animals. For this purpose, all muscles were detached from the upper end of the femur (carefully preserving the nerve and blood supply to the hip joint), and a subtrochanteric femoral osteotomy was then performed. After fixation of the pelvis to the scaffold attached to the operating table, passive movements of the isolated head of the femur within the acetabulum were performed in all directions by manipulation of a rod fixed into the proximal femoral stump. The angle of movement of the femur was measured using double exposure photography; and as the static posture of the limbs could be altered by adjusting the position of the fixation pin transfixing both upper tibiae, it was possible to compare the results of passive hip joint movements initiated from different rest positions of the joint.

Figure 9 (a) shows the pattern of reflex responses obtained when the mechanoreceptors in the inferior regions of the capsule of the hip joint are stimulated by abduction of the femoral stump. The most noticeable effect in these circumstances is the reciprocally coordinated change in the tone of the adductor and abductor musculature: for there is considerable inhibition of the activity of the gluteus medius muscles, most marked ipsilaterally, that is accompanied by adductor facilitation. When the femur is returned to the resting position, the inhibition of the gluteal activity disappears (Fig. 9b). The capsular origin of these reflexes is confirmed by the fact that they are totally abolished by infiltration of the joint capsule with 1 per cent Lignocaine, by performance of capsulectomy, or by section of the relevant articular nerves.

The pattern of response evoked during flexion-extension movements of the joint has also been studied. During flexion there is an initial brief facilitatory burst of motor unit activity in the rectus muscles (presumably a result of transient Type II receptor discharge) and then a gradual diminution in the tone of the psoas muscles as the proximal femoral stump is moved into full flexion. These changes in flexor muscle activity are reversed when the proximal femoral stump is moved into extension. Most of the activity in this example, in which the limbs were initially in 60° of flexion, occurred in the flexor muscles; but when the limbs were flexed to 90° the response in the flexor musculature was much less, and reciprocally coordinated activity in the biceps femoris muscles was seen instead. This is because altering the relative tension distribution in the various regions of the hip joint capsule changes the resting afferent discharge from the Type I receptors therein, and consequently their regional sensitivity to additional mechanical stimulation.

After capsulectomy, however, a different pattern of reflexes is provoked when the head of the femur is pressed firmly into the acetabulum to stretch and compress the ligamentum capitis femoris. Generalized inhibition of varying degrees now results in all muscle groups (with the exception of the glutei, which are facilitated in these circumstances instead of being inhibited). This response is comparable to that obtained by direct electrical stimulation of the nerve to the ligamentum capitis femoris. The inhibition lasts for as long as the impressive force is maintained; and when the impression is released, there is immediate rebound facilitation in the previously inhibited muscles that lasts some two seconds before the normal static postural pattern of motor unit activity is restored.

In contrast to these results, distraction of the joint has little reflex effect; and even when the head of the femur is subluxated from the joint, reflex changes are minimal. When the acetabular attachment of the ligament is directly compressed with the end of a glass rod after excision of the femoral stump, however, typical generalized inhibitory reflex responses are elicited; and these again are followed by powerful rebound facilitation when the pressure is released.

The origin of these inhibitory reflexes from mechanoreceptors located in the ligamentum capitis femoris is confirmed by the fact that they are totally abolished by direct infiltration of the ligamentum capitis femoris with 1 per cent Lignocaine, but only if the whole of the acetabular origin of the ligament is injected. They are also totally abolished by selective section of the nerve to the ligament, and are readily suppressed by a moderate increase in the degree of general anaesthesia. Comparable reflexes were not elicitable by direct compression of the Haversian fat pad, the transverse acetabular ligament, or the articular cartilage of the hip joint.

We are now in the process of quantifying the role of these reflexes elicitable from the receptors in the ligamentum capitis femoris, but it seems likely, in the light of our current neurohistological and neurophysiological observations, that one of the principal functions of this ligament is reflexogenic. The ligament is liberally provided with high threshold Type III mechanoreceptors; and it seems clear that their discharges are capable of exerting powerful reflex effects that are predominantly inhibitory and which involve the hip joint musculature on both sides of the body, with the possible exception of the ipsilateral abductors (which are commonly facilitated). It remains to be seen whether these reflexes are brought into play during normal physiological movement; but it should be recalled that Rydell (1966) found (using a strain-gauge prosthesis during running) that in the support phase of the leg movement forces up to five times the body weight could be recorded. It would certainly seem probable that this system represents a protective reflex, acting to cause profound inhibition of the adductors and associated muscles around the hip (with abductor facilitation) when the impressive forces across the joint are such that a fracture of the femoral neck might otherwise result.

Certainly, the capsular mechanoreceptor reflexes, which operate in response to lesser degrees of mechanical stress in the joint tissues, are modified when the reflexes originating from the mechanoreceptors in the ligamentum capitis femoris are brought into play as well. Thus, during manipulation of a neurologically intact joint, when the capsular reflex alone is provoked, the glutei are inhibited in abduction movements; but when the reflex from the ligamentum capitis femoris is elicited by compression, there is gluteal facilitation. If this compression be maintained, abduction movements now cause a further increase in gluteal facilitation that continues until the fully abducted position is reached. As soon as the impressive force is removed, the capsular reflex alone is unmasked and characteristic abductor inhibition now appears. 

CONCLUSION 

In the light of the anatomical and histological studies that I have presented, it seems reasonable to conclude that the hip joint, like all the other limb joints that have been examined in our laboratory, is liberally provided with an array of mechanoreceptor and pain receptor nerve endings that are innervated by afferent fibres reaching the various regions of the joint capsule and the ligamentum capitis femoris from specific articular branches of the nerve trunks entering the limb. Furthermore, the regional distribution and population densities of the various types of mechanoreceptors in the hip joint (for example, the relative proportions of Type I and Type II end-organs) correlate well with our interpretation of the various functions of these nerve endings in our previous studies of other limb joints; and I hope that our neurophysiological investigations have established that discharges traversing the articular afferent nerve fibres exert reflexly coordinated facilitatory and inhibitory influences bilaterally on the muscles operating over the hip joint.

Goldscheider (1889) long ago recognized that the joint mechanoreceptors hold pride of place in conscious appreciation of limb position and movement (apart from vision); but their importance in the reflex regulation of muscle tone is only now becoming recognized (Wyke, 1967). In clinical practice, the antalgic posture* of the patient with early tuberculosis of the hip; the fixed flexion deformity associated with a slipped capital epiphysis (accompanied by an extension deformity of the bone); the 'shortening of the adductors' of some cases of congenital dislocation of the hip; and, perhaps most common of all, the flexed adducted deformity produced by osteo-arthrosis of the hip, are gross examples of the variety of postural abnormalities that may be seen in cases of advanced hip joint pathology. But the changes in muscle function may be more subtle than in these grossly abnormal states in the early stages of disease; and it is to these early abnormalities of muscle function that occur before gross alterations in structural anatomy develop to distort the situation that I would like finally to direct your attention. 

* I.e., the involuntary posture taken up to relieve pain. Often this is abduction. 

For example, Figure 10 shows a patient aged 21, who was admitted for investigation of an ' irritable hip '. She had had pain in the right groin and an ache in the whole of the right leg for two weeks prior to admission; but she had also noticed that for three years prior to admission her right hip had occasionally given way when rising from a chair, or when standing. On admission she was tender over the right inguinal region, and all movements of the right hip joint were slightly limited by pain. Although her erythrocyte sedimentation rate was 40 mm/hr. and her temperature on admission was 1000 F, her serological and blood culture investigations were negative and she remained undiagnosed. Nevertheless, with continued rest her pain disappeared over the next three weeks.

When examined four months later she had no complaint of any kind, apart from some pain and limitation of movement now in both temporomandibular joints-which suggested that she might be an early case of seronegative rheumatoid arthritis. Routine clinical examination of the hip on this occasion revealed no significant abnormality. Her sedimentation rate had fallen, and her radiographs remained normal. However, specific examination of kinaesthetic sensation in her right hip revealed an obvious impairment; and when her visual righting reflexes were obliterated by masking her eyes, a marked abnormality of postural reflexes in the right lower limb became clearly manifest (Fig. 10).

In the light of observations such as these, then, we would like to suggest that a lesion of the hip joint which alters the complex reflex feed-back from the receptors in the hip joint capsule will not only affect perceptual awareness of static hip joint position and of hip joint movement, but will also-alter the reflex adjustment of tone in the muscles around the joint that are normally contributed from the mechanoreceptors that we have shown to be present in the articular tissues of the hip. Whether such neurological changes play a clinically significant role in the symptomatology or the development of joint disease is not yet clear; but I hope that the material that I have been privileged to present in this Arnott Demonstration suggests that such a hypothesis merits consideration by orthopaedic surgeons and specialists in physical medicine. 

ACKNOWLEDGEMENTS 

I wish to thank the Trustees of the Camilla Samuel Fund for their financial support of this research project; Dr. Wyke for his help and advice in the preparation of this paper; and Mr. C. Redman for the photographs. 

REFERENCES 

BLAND-SUTTON, J. (1883) J. Anat., Lond. 17, 191.

FREEMAN, M. A. R., and WYKE, B. D. (1966) Brit. J. Surg. 53, 1.

- (1967a) Brit. J. Surg. 54, 12.

- (1967b) J. Anat., Lond. 101, 505.

- (1967c) Acta anat., Basel, 68, 321.

GOLDSCHEIDER, A. (1889) Arch. Anat. Physiol. Leipzig, 13, 369.

GREENFIELD, B. E., and WYKE, B. D. (1966) Nature, Lond., 211, 5052.

KIRCHNER, J. A., and WYKE, B. D. (1965) Ann. Otol. Rhinol. Laryngol. 74, 749.

POLAUEK, P. (1963) Anat. Anz. 13, 369.

RYDELL, N. (1966) In Studies of the Anatomy and Function of Bone and Joints. New York, Springer.

WYKE, B. D. (1967) Ann. Roy. Coll. Surg. Engl. 41, 7.



Fig. 1. (a) Dissection of the left posterior articular nerve in a cat. (A) Head of femur; (B) nerve branches to posterior capsule; (C) nerve branch to inferior capsule; (D) muscular branch to quadratus femoris muscle; (E) quadratus femoris muscle; (F) inferior gluteal nerve; (G) acetabular fringe of posterior joint capsule; (H) branch to superior capsule; (I) nerve to quadratus femoris (musculo-articular nerve).

(b) Dissection of the right medial articular nerve in a cat. (A) Anteromedial hip joint capsule; (B) right medial articular nerve; (C) pectineus muscle; (D) obturator foramen; (E) obturator externus muscle; (F) anterior right obturator nerve; (G) adductor magnus muscle.


Fig. 2. (a) Dissection of the nerve to the right ligamentum capitis femoris in a cat. (A) Acetabular notch; (B) inferior joint capsule; (C) calcar femorale; (D) articular nerve to the ligament; (E) nerve trunk arising from posterior division of the obturator nerve; (F) muscular nerve to obturator externus muscle.

(b) Dissection of the accessory articular nerve from the nerve to the left pectineus muscle in a cat. (A) Left pectineus muscle; (B) nerve to pectineus muscle; (C) branch to joint capsule; (D) anterior joint capsule; (E) left psoas muscle; (F) femoral nerve (main branch).


Fig. 3. The principal categories of nerve endings in articular tissues of the hip joint. (Fitzgerald frozen silver technique.) (Magnifications indicated by scales.) (a) Type I cluster on a single myelinated nerve fibre (cat inferior capsule). (b) A single Type II ending (human posterior capsule). (c) Asingle Type III ending on the surface of the ligamentum capitis femoris (human). (d) Plexus of unmyelinated nerve fibres beneath the surface of posterior joint capsule. 


Fig. 4. Multichannel electromyographic recording during stimulation of the right medial articular nerve. (Stimulus applied for 3 sec at S.) 


Fig. 5. Effects of stimulation of the left posterior articular nerve (branch to postero-superior capsule). (Stimulus applied for 3 sec at S.)

 

Fig. 6. Effects of stimulation of the left posterior articular nerve (branch to postero-inferior capsule). (Stimulus applied for 3 sec at S.)

 

Fig. 7. Effects of stimulation of the nerve to right ligamentum capitis femoris. (Stimulus applied for 3 sec at S.)

 

Fig. 8. Effects of stimulation of the same nerve as in Fig. 7, but at higher voltage. (Stimulus applied for 3 sec at S.)

 

Fig. 9. (a) and (b) Effects of passive movement of isolated upper femoral stump in acetabulum. (Joint capsule and ligaments intact.) (For explanation see text.)



Fig. 10. Persisting impairment of postural reflexes in a patient after apparent recovery from an 'irritable hip' on the right side. Solid line- true vertical axis. Vertical broken line body axis. Oblique hatched lines indicate axis of nonsupporting leg. (Description in text.)


Dee R. Structure and function of hip joint innervation. Ann R Coll Surg Engl. 1969;45(6)357-74.  ncbi.nlm.nih.gov , pmc.ncbi.nlm.nih.gov/pdf , PMCID: PMC2387679 ,  PMID: 5359432


The work is cited in the following publications: Нервы и рецепторы LCF человека. Обзор , Функция ритмовводителя, присущая LCF. Обзор , Чувствительная функция LCF. Обзор

Article from Annals of The Royal College of Surgeons of England are provided here courtesy of The Royal College of Surgeons of England


Roger Dee, M.A., F.R.C.S. Neurologcal Laboratory, Royal College of Surgeons of England, and Department of Orthopaedic Surgery, Middlesex Hospital, London


ligamentum capitis femoris, ligamentum teres, ligament of head of femur, anatomy, nervous system, nerve, structure, role, biomechanics



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