The role of joint afferents in sensory processing in osteoarthritic knees

H.-T. Weiler, G. Pap and F. Awiszus

Otto-von-Guericke-Universität Magdeburg, Neuromuscular Research Group at the Department of Orthopaedics, Leipziger Strasse 44, 39120 Magdeburg, Germany


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Objective. To test the role of joint receptors for proprioception in patients with bilateral knee osteoarthritis (OA) and patients who had undergone unilateral total knee arthroplasty (TKA).

Methods. Nine patients were tested bilaterally with a conventional movement detection paradigm that evaluated conscious detection perception and a newly developed hunting paradigm that measured maximal sensory performance (hunting perception).

Results. For detection perception, patients exhibited a slightly lower threshold on the arthritic side than on their TKA side. For hunting perception, the patients showed threshold values that were an order of magnitude smaller than for the conventional paradigm in both knees. Performance was much better on prosthetic knees than on OA knees.

Conclusion. The joint receptors of OA knees might have an adverse effect on the maximal proprioceptive performance, being important for the normal reflexive knee joint functions. These deficits may be overcome by joint receptor removal during knee replacement.

KEY WORDS: Proprioception, Total knee arthroplasty, Osteoarthritis, Knee, Joint receptors, Movement detection.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
The proprioceptive performance of patients suffering from osteoarthritis (OA) of the knee joints has been described in several publications as mild to severely impaired [15]. Impaired proprioception has been hypothesized as one of several reasons for the initiation and progression of osteoarthritis [2, 48]. The increasing pain and disability caused by knee osteoarthritis often leads to radical operative intervention in the form of total knee arthroplasty (TKA). Recent publications have referred to the importance of sparing joint receptors in TKA [1, 9, 10]. This is surprising, since muscle spindles and not joint receptors have been seen as the most important components of the proprioceptive system [1115]. Joint receptors respond preferably at extreme joint positions. Muscle spindles register the information regarding body position and motion that is necessary for smooth movements.

Thus, the question arises of the role of joint receptors in proprioceptive performance in OA. Is their presence in OA of benefit and should their removal be prevented in TKA as far as possible? In order to answer these questions, we have investigated proprioceptive performance with a commonly used movement detection test [1622]. The difference in angular degrees between the real and perceived onset of movement (about 1°) in this threshold detection test can be seen as a measure of one aspect of proprioceptive performance, detection perception.

Recently, we have developed a new way to measure the threshold of movement detection using a threshold hunting paradigm. The paradigm revealed very small threshold values for angular displacement. Healthy adult subjects showed a threshold value of 0.1° with movement velocities of 0.1° s-1 [23]. Given that muscle spindles are the receptors responsible for movement detection, for theoretical reasons movements of 0.01° should be detectable [24, 25]. Thus the performance measured with the hunting paradigm reflects more the performance of the receptors than the outcome of the central processing of the sensation. In other words, this measure, values for which were one order of magnitude smaller than those for detection perception performance, reflects a performance that is more related to an earlier state in the sensory order of perception [26, H.-T. Weiler and F. Awiszus, submitted for publication]. Differences in vulnerability in different states should give insight into the nature of the role of joint afferents in sensory processing in OA patients.

Therefore, the present study investigated the proprioceptive performance of patients with two OA knees, one with joint receptors and one without (TKA), using two methods of evaluating the detection of movement.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Subjects
Proprioceptive detection performance was evaluated in nine patients with bilateral OA. The mean age of this group was 66.6 ± 1.5 (S.E.M.) yr, and there were two males and seven females. One of the knees of each patient had received TKA (Natural Knee®, Sulzer Orthopedics, five right and four left knees). The interval after TKA at the time of testing was 62.2 ± 2.0 months (mean ± S.E.M.; range 54–69 months). For the other knee, all subjects fulfilled the following clinical criteria of the American College of Rheumatology (ACR) classification for OA of the knee: knee pain on most days of the previous month; crepitus; morning stiffness lasting >30 min; and age over 60 yr [27, 28]. The patients' knee conditions were also evaluated with the Knee Society's knee score (i.e. subscore A) [29]. Both knee joints, the operated and the OA knee, were tested. Subjects were tested first with the movement detection paradigm and then with the threshold hunting paradigm. The study was conducted with the informed consent of the subjects and with approval of our institution's ethics committee.

The subject was instructed to relax the muscles of the test joint completely, and to concentrate on possible movements of the knee. To avoid external clues, the apparatus and the knee joints were screened from the subject's vision and white noise was delivered via headphones.

Apparatus
The subject sat on a comfortable armchair with the legs hanging freely over the side of the seat. The foot and ankle of the leg being investigated were immobilized with a rigid inflated air splint reaching up to 10 cm distal to the knee joint. The splint was suspended and connected by a wire to a stepper motor. An internal pressure of 4 kPa (30 mmHg) in the splint ensured that the ankle remained fixed, whilst not occluding circulation. A second air cuff was used 10 cm proximal to the knee joint. The purpose of the cuffs was to minimize cutaneous sensation.

The test rig consisted of a metal frame in front of the subject. A winding drum was connected to the stepper motor at the top of the frame. As the stepper motor moved, the wire wound up (in the case of extension) and pulled the shank and foot upwards. The drive system was covered with a screen. The screen showed three coloured light signals (red, yellow and green). The speed and direction of turning of the motor were software-controlled by an intelligent controller (Röbe-Oltmanns-Systeme, Apen, Germany).

The contralateral shank was not fixed and could be moved freely. Since the leg was moved along a line corresponding to the arc of motion, the displacement in millimetres could be converted accurately to angular displacement.

No vibrations could be detected with a highly sensitive accelerometer placed at the position of the seat, the subject, or anything else the subject was in contact with during the session.

Procedures
Go/stop detection paradigm.
The procedure was that of Pap et al. [22, 30]. The subjects' performance in the detection of movement onset and offset was tested six times for each knee joint. Each run was announced separately by the experimenter. The patient pressed the button of a computer mouse when he or she detected the onset or offset of movement. After the subjects' decision, the joint was returned to the starting position (45°). The values for angular displacement were stored on the hard disk of the computer after each run. Movements consisted of flexion or extension with equal probability and always with the same angular velocity of 0.6° s-1.

Threshold hunting paradigm.
The procedure was that of Weiler and Awiszus [23]. Data are presented for specific amplitude hunting with respect to flexion. During amplitude hunting, the angular velocity is held constant and the angular displacement (amplitude) of the stimulus movement is varied depending on the subject's response. The subject was required to detect flexions between imposed flexions, extensions and sham movements (no movement). Thus, a flexion was the stimulus and the sham stimulus an extension or a sham movement. The correct detection of the direction of movement is important, as in many basic research publications the term ‘proprioception’ has been used properly only when the subjects have been able to report the direction of the imposed movement [14, 17, 24, 25, 3134].

Each run was started by a warning interval identified by a red light signal on a screen, indicating that after a short time (4 s) a movement may start, consisting of a flexion or an extension. During the subsequent observation interval, identified by a yellow light signal, the movement or sham movement was imposed. The order of testing for stimuli (flexions) and sham stimuli (extensions and sham movements) was distributed randomly with a probability of 0.5 for stimuli and sham stimuli. Within sham stimuli, the order of testing for extensions and sham movements was also distributed randomly with equal probability. Sham movements were intervals of no motions with a duration as long as related motions in test. A green light signal that appeared 500 ms after cessation of the observation interval indicated that the subject had to decide, without a time limit, whether a flexion had occurred during the yellow light period. Depending on this decision, a button had to be pressed. Immediately after the subject had made the decision, the joint was returned to the starting position (45°) at the rate of 1° s-1 and the green light signal disappeared. The resetting movement was fast enough to be perceived clearly most of the time. If the response was correct, the yellow and green signals lit up briefly and thus served as reinforcement. If the response was wrong the yellow and red signals lit up. After each run the value of the amplitude that had been tested was stored. If the subject failed to detect a stimulus or sham stimulus correctly twice within three successive trials, the amplitude was increased. Such a change was associated with a change in the direction of the ‘hunting curve’ towards higher amplitude values by one step, according to the amplitude level tested. The corresponding value was stored in a temporary file as the minimal amplitude value. Otherwise, when more than one decision within the previous three trials was correct the amplitude was decreased by one step corresponding to the amplitude level tested. The amplitude step size was 0.01° when the amplitude was lower than 0.15°, 0.02° when it was lower than 0.25°, 0.05° when it was lower than 0.5°, 0.1° when it was lower than 1°, 0.25° when it was lower than 2°, and 0.5° when it was lower than or equal to 5°. The next run started 3 s later. One test session consisted of 50 trials. The detection performance for flexions was tested for an angular velocity of 0.6° s-1 with a starting amplitude of 1°.

All hunting curves could be clearly distinguished from those that would result from guessing by means of Monte Carlo simulations described in detail elsewhere [23].

Data analysis
Go/stop detection paradigm.
The distributions of the values of angular displacement for go and stop detection for prosthetic and OA knee joints were compared by the use of the Kolmogorov–Smirnov test. The threshold values of angular displacement for go and stop detection (median of the six values) were compared by the use of the Mann–Whitney rank sum test.

Hunting paradigm.
The distributions of the values for the tested angular displacements for prosthetic and OA knee joints were compared by the use of the Kolmogorov–Smirnov test. Individual hunting curves were analysed as described proviously [23]. The median of the minimal amplitude values, stored in a temporary file, which characterizes changes during the course of hunting towards larger values, was computed as the threshold value at the end of the session and was stored in a results file. Fifty trials were used to produce a stable hunting curve. More trials would not have improved the result because fatigue would have occurred. The first 15 values of an individual hunting curve were disregarded as these might have reflected training effects.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
The subjects had a median knee score of 88 (range 80–99). More pain was reported in the OA knee than in the TKA knee (TKA, median = 50; OA, median = 40; P = 0.03). No differences were reported between the two knees in muscle strength or fatigue. There was no correlation between pain and any other parameter tested (P = 0.11–0.82, Spearman rank order correlation).

Figure 1Go shows two hunting curves that are qualitatively similar but quantitatively represent the extremes. Figure 1AGo and BGo show results for a single 60-yr-old female patient. The detection of movement onset was earlier and more homogeneous for the OA knee (filled circles) than for the prosthetic knee (open circles) in the movement detection paradigm (Fig. 1AGo). The patient's hunting curve shows that she very consistently detected very small movements with her prosthetic knee but not with the OA knee (Fig. 1BGo). The shape of the curve shows two parts; the initial pattern is very similar for the two knees, since the patient reached a similar detection level with her two knees. The second part of the curve shows that with the OA knee she was unable to reach the level she attained with the prosthetic knee. Figure 1CGo and DGo show results for another 66-yr-old female patient. Whereas the results of the movement detection paradigm were very similar to those for the first patient (Fig. 1CGo), the shapes of the hunting curves differ drastically quantitatively, but not qualitatively (note the different ordinate scales) (Fig. 1DGo).



View larger version (19K):
[in this window]
[in a new window]
 
FIG. 1. Results for a 60-yr-old female patient. (A) The continuous line is the curve for a passive movement imposed on the knees six times (angular displacement 10°, angular velocity 0.6° s-1). The distribution of the times at which the onset of movement was detected is given above the curve for the OA knee (filled circles) and the prosthetic knee (open circles). (B) The same patient's hunting curve, derived from 50 angular displacement values tested consecutively in a threshold hunting paradigm. (C and D) Corresponding results for a 66-yr-old female patient. Note the different ordinate scales in B and D.

 
The results for the remaining patients were quantitatively more similar to those of the first patient than to those of the second patient. As can be seen in Fig. 2AGo, the distributions of the go detection values for all patients in the conventional movement detection paradigm for the OA side (continuous lines) were significantly different from the distributions for the TKA side (dashed line) (P = 0.001). A similar difference was found for the stop detection values (P < 0.001). On both sides, the go detection values did not differ from the stop values (P = 0.21 and 0.70). The distributions of amplitude values for the threshold hunting paradigm shown in Fig. 2BGo showed an opposite behaviour (P < 0.001).



View larger version (14K):
[in this window]
[in a new window]
 
FIG. 2. Cumulative distribution functions for values for all patients (n = 9) for two different paradigms measuring proprioceptive performance on the OA side (continuous line) and the TKA side (dashed line). Patients were tested with a conventional movement detection paradigm measuring detection perception. (A) Cumulative distribution functions, of the time intervals at which movement onset (go detection) was detected. (B) Cumulative distribution functions of the tested angular displacement values for a threshold hunting paradigm measuring hunting perception.

 
The threshold values for the two paradigms are depicted in Fig. 3Go. The go detection threshold values (the median value of each individual leg) were slightly but significantly smaller on the OA side (median 1.12°, first quartile 0.94°, third quartile 1.24°) than on the TKA side (median 1.49°, first quartile 1.24°, third quartile 1.89°) (P = 0.027; Fig. 3AGo). The stop detection threshold values exhibited no statistically significant difference (P = 0.331; Fig. 3BGo). For both knees, the threshold values of the hunting paradigm were an order of magnitude smaller compared with the conventional movement detection paradigm. However, the threshold on the OA side (median 0.40°, first quartile 0.35°, third quartile 0.50°) was on average twice as large as the threshold on the TKA side (median 0.19°, first quartile 0.13°, third quartile 0.26°) (P = 0.024; Fig. 3CGo).



View larger version (10K):
[in this window]
[in a new window]
 
FIG. 3. Threshold values (median plus third quartile), based on the distributions of the two paradigms depicted in Fig. 2Go, for the OA side (filled columns) and the TKA side (open columns). (A) Detection perception in the conventional movement detection paradigm for movement onset (go detection). (B) Detection perception in the conventional movement detection paradigm for movement offset (stop detection). (C) Hunting perception in the threshold hunting paradigm.

 


    Discussion
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Since proprioceptive performance was attributed to muscle spindles, all factors affecting the muscles could have affected the results. It is conceivable that the consequences of surgery, e.g. improved ambulation, intensive physical therapy, and therefore improved muscle strength and decreased pain, might have influenced the results. No consistent differences were found in muscle strength between the two knees in brief clinical tests, although more objective and precise testing of muscle function, e.g. using the twitch interpolation technique, would be desirable [35, 36]. Patients reported no differences in fatigue. Self-reported fatigue might not be a sufficient criterion since muscle fatigue, a well researched area, has a well characterized methodology [37]. Because of the method we used to select the patients for the study, pain was reported more on the OA side than on the TKA side. Pain might increase the level of background firing of {gamma}-motor neurons [38] and thereby increase the sensitivity of the muscle spindles. However, in a recent study in cats, increased {gamma}-innervation was shown to be deleterious to proprioception [39]. Nevertheless, the pain score did not correlate significantly with any of the parameters that were measured. During test sessions no pain was reported and no analgesics were used. Therefore, despite methodological weaknesses in the measurement of muscle strength, fatigue and pain, even if there had been a difference in one of these parameters, this difference can explain, if indeed it can explain anything, the results found in either of the two paradigms, but not the dissociation between them.

Before discussing the results, it should be pointed out that not only were the hunting perception and detection perception values different in magnitude, but their trends followed opposite directions. Therefore, we can exclude the possibility that they were simply a phenomenon of scaling; they were qualitatively different. Moreover, the two sets of measurements were made with the same apparatus. Thus, possible differences cannot be attributed to different technical arrangements, since only the patients' tasks were different.

Obviously, the standard perception test used to characterize detection perception performance [1619] does not reflect the maximal performance level of the receptors in the periphery. Results of this test might be influenced to a large extent by some kind of cognitive processing, as has also been shown in a previous investigation [40].

The side differences found for the group of patients investigated here were conflicting. Considering the performance in detection perception of the present results, at first glance one may assume that the presence of joint receptors may be of benefit for the perception of passive motion, a result clearly in line with those of other groups [1, 10]. The most obvious explanation for this finding would be that joint receptors contribute in some way to the perception of passive motion. This simple hypothesis, however, was refuted by our results, in that the knees lacking joint receptors had a clearly lower hunting perception threshold than OA knees, which had joint receptors. Consequently, basic motion perception does not require the presence of joint receptors and even appears to be impaired by their presence. This would add some evidence to the hypothesis of abnormal afferent signals produced by joint receptors in OA knees that are thought to be responsible for the arthrogenous quadriceps weakness of these patients [2, 8]. This also explains the excellent clinical outcome of the knee replacement operation with a type of prosthesis that is not intended to spare receptors of any kind.

As joint-receptor-mediated perceptions can be excluded as the reason for the better detection perception performance of the receptor-bearing knee, there must be another explanation. First, one must consider that the replaced knee had been the clinically worse joint before the operation. Thus, it may well be the case that a larger perception deficit was present in the replaced knee before surgery and that this deficit had not vanished even after 5 years. Loss of sensory information leads to cortical reorganization, as is well known from studies in amputees [41]. A correlation of clinical state with proprioceptive performance has been described for OA patients [2, 48]. Interestingly, the presence of a side difference in performance in the perception of passive motion has been found to be highly correlated with a permanent central representation change of cortical potentials in patients with chronic deficiency of the anterior cruciate ligament [42]. Similar permanent cortical reorganization in our prosthetic patients would explain the observation that perception deficits may be present to an even greater extent when the knee is replaced.

As a second hypothesis, it may be assumed that joint receptor afferents, even if altered by chronic OA, may perform some kind of central gating for the perception of passive motion. Removal of these receptors by knee replacement would impair the gating mechanism, resulting in reduced performance in detection perception despite normal hunting perception.

As the joint receptors were completely removed on the TKA side, they can be excluded as a source of information. Therefore, the most probable information source for the measured hunting perception performance appears to be the muscle receptors, particularly the muscle spindles. Thus, the difference lies in the alteration in muscle physiology and function that accompanies knee replacement and subsequent rehabilitation. Thereby, improved ambulation and intensive physical therapy should improve muscle function bilaterally rather than just unilaterally. Unfortunately, not enough is known about muscle function to allow an explanation of this hypothesis. This, together with the objective measurement of pain and fatigue, should be the subject of further studies.

In summary, our results were contradictory. On the one hand, sensory sensation in replaced knees was not reduced peripherally, so that hunting perception (maximal proprioceptive performance) was still possible, and joint receptors were not responsible for this performance. Without joint receptors the central proprioceptive processing of perception appeared to be slightly disturbed. On the other hand, OA knees showed impaired hunting perception performance. Thus, the joint receptor of the OA knee might have an adverse effect on hunting perception even when it has an improving effect on central processing. Since the effect of joint receptors on {gamma}-motor neurons has been demonstrated [43], the adverse effect of the ‘OA joint receptor’ might be seen in this function. Therefore, the removal of such altered receptors by TKA appears to be beneficial, because the maximal proprioceptive performance tested by the hunting paradigm may be important for reflexes and the physiology of gait. When making decisions about intervention, one has to choose between the preservation of the joint receptors in order to improve or preserve central processing, and their removal in order to improve or preserve maximal proprioceptive performance.


    Acknowledgments
 
This work was supported by the Deutsche Forschungsgemeinschaft (Aw5–2/2).


    Notes
 
Correspondence to: H.-T. Weiler, Otto-von-Guericke-Universität Magdeburg, Medizinische Fakultät, Orthopädische Universitätsklinik, Forschungsabteilung, Leipziger Strasse 44, 39120 Magdeburg, Germany. Back


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

  1. Barrett DS, Cobb AG, Bentley G. Joint proprioception in normal, osteoarthritic and replaced knees. J Bone Joint Surg1991;73B:53–6.
  2. Hurley MV, Scott DL, Rees J, Newham DJ. Sensorimotor changes and functional performance in patients with knee osteoarthritis. Ann Rheum Dis1997;56:641–8.[Abstract/Free Full Text]
  3. Marks R, Quinney HA, Wessel J. Proprioceptive sensibility in women with normal and osteoarthritic knee joints. Clin Rheumatol1993;12:170–5.[ISI][Medline]
  4. Pai YC, Rymer WZ, Chang RW, Sharma L. Effect of age and osteoarthritis on knee proprioception. Arthritis Rheum1997;40:2260–5.[ISI][Medline]
  5. Sharma L, Pai YC, Holtkamp K, Rymer WZ. Is knee joint proprioception worse in the arthritic knee versus the unaffected knee in unilateral knee osteoarthritis? Arthritis Rheum1997;40:1518–25.[Medline]
  6. Sharma L, Pai YC. Impaired proprioception and osteoarthritis. Curr Opin Rheumatol1997;9:253–8.[Medline]
  7. Slemenda C, Brandt KD, Heilman DK et al. Quadriceps weakness and osteoarthritis of the knee. Ann Intern Med1997;127:97–104.[Abstract/Free Full Text]
  8. Hurley MV Quadriceps weakness in osteoarthritis. Curr Opin Rheumatol1998;10:246–50.[Medline]
  9. Attfield SF, Wilton TJ, Pratt DJ, Sambatakakis A. Soft-tissue balance and recovery of proprioception after total knee replacement. J Bone Joint Surg Br Vol1996;78:540–5.[Medline]
  10. Warren PJ, Olanlokun TK, Cobb AG, Bentley G. Proprioception after knee arthroplasty. Clin Orthop Rel Res1993;297:182–7.[Medline]
  11. Gandevia SC, Burke D. Does the nervous system depend on kinesthetic information to control natural limb movements? Behav Brain Sci1992;15:614–32.[ISI]
  12. Gandevia SC, McCloskey DI, Burke D. Kinaesthetic signals and muscle contraction. Trends Neurosci1992;15:62–5.[ISI][Medline]
  13. Matthews PBC. Where does Sherringtons's ‘muscular sense’ originate? Muscles, joints, corollary discharges? Annu Rev Neurosci1982;5:189–218.[ISI][Medline]
  14. McCloskey DI. Kinesthetic sensibility. Physiol Rev1978;58:763–820.[Free Full Text]
  15. Sherrington CS. On the proprioceptive system, especially in its reflex aspects. Brain1906;29:467–82.
  16. Pillsbury WB. Does the sensation of movement originate in the joint? Am J Psychol1901;12:346–53.
  17. Laidlaw RW, Hamilton MA. The quantitative measurement of apperception of passive movement. Bull Neurol Inst N Y1937;6:145–53.
  18. Barrack RL, Skinner HB, Cook SD, Haddad RJ. Effect of articular disease and total knee arthroplasty on knee joint-position sense. J Neurophysiol1983;50:684–7.[Abstract/Free Full Text]
  19. Skinner HB, Barrack RL, Cook SD, Haddad RJ. Joint position sense in total knee arthroplasty. J Orthop Res1984;1:276–83.[Medline]
  20. Hall MG, Ferrell WR, Baxendale RH, Hamblen DL. Knee joint proprioception: threshold detection levels in healthy young subjects. Neuro-Orthopedics1994;15:81–90.
  21. Hall MG, Ferrell WR, Sturrock RD, Hamblen DL, Baxendale RH. The effect of the hypermobility syndrome on knee joint proprioception. Br J Rheumatol1995;34:121–5.[ISI][Medline]
  22. Pap G, Machner A, Awiszus F. Messung der Kniegelenkskinästhesie zur Bestimmung von Propriozeptionsdefiziten bei Varusgonarthrose. Z Rheumatol1998;57:5–10.
  23. Weiler H-T, Awiszus F. Characterization of human joint proprioception by means of a threshold hunting paradigm. J Neurosci Methods1998;85:73–80.[ISI][Medline]
  24. Refshauge KM, Chan R, Taylor JL, McCloskey DI. Detection of movements imposed on human hip, knee, ankle and toe joints. J Physiol (Lond)1995;488:231–41.[Abstract]
  25. Refshauge KM, Fitzpatrick RC. Perception of movement at the human ankle: effects of leg position. J Physiol (Lond)1995;488:243–8.[Abstract]
  26. Weiler H-T, Awiszus F. Nonspecific velocity and amplitude hunting reveals different specific detection performance of flexion and extension movements in the human knee joint. Exp Brain Res2000;131:375–80.[ISI][Medline]
  27. Hart DJ, Spector TD. The classification and assessment of osteoarthritis. Baillieres Clin Rheumatol1995;9:407–32.[ISI][Medline]
  28. Altman R, Asch E, Bloch D et al. Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum1986;29:1039–49.[ISI][Medline]
  29. Insall JN, Dorr LD, Scott R, Scott WN. Rationale of the Knee Society clinical rating system. Clin Orthop1989;248:13–4.[Medline]
  30. Pap G, Machner A, Nebelung W, Awiszus F. Detailed analysis of proprioception in normal and ACL-deficient knees. J Bone Joint Surg Br1999;81:764–8.[Medline]
  31. Hall LA, McCloskey DI. Detection of movements imposed on finger, elbow and shoulder joints. J Physiol (Lond)1983;335:519–33.[Abstract]
  32. Laidlaw RW, Hamilton MA. A study of thresholds in apperception of passive movement among normal control subjects. Bull Neurol Inst N Y1937;6:268–73.
  33. Goldscheider A. Untersuchungen über den Muskelsinn. Arch Anat Physiol1889;3:369–502.
  34. Gandevia SC, McCloskey DI. Joint sense, muscle sense, and their combination as position sense, measured at the distal interphalangeal joint of the middle finger. J Physiol (Lond)1976;260:387–407.[Abstract]
  35. Bülow PM, Norregaard J, Danneskiold-Samsoe B, Mehlsen J. Twitch interpolation technique in testing of maximal muscle strength: influence of potentiation, force level, stimulus intensity and preload. Eur J Appl Physiol1993;67:462–6.
  36. Rutherford OM, Jones DA, Newham DJ. Clinical and experimental application of the percutaneous twitch superimposition technique for the study of human muscle activation. J Neurol Neurosurg Psychiatry1986;49:1288–91.[Abstract]
  37. Vollestad NK. Measurement of human muscle fatigue. J Neurosci Methods1997;74:219–27.[ISI][Medline]
  38. Matre DA, Sinkjaer T, Svensson P, Arendt-Nielsen L. Experimental muscle pain increases the human stretch reflex. Pain1998;75:331–9.[ISI][Medline]
  39. Wise AK, Gregory JE, Proske U. The responses of muscle spindles to small, slow movements in passive muscle and during fusimotor activity. Brain Res1999;821:87–94.[ISI][Medline]
  40. Weiler H-T, Awiszus F. Characterization of human knee joint proprioception by means of signal detection theory. Soc Neurosci Abstr1997;27:2342.
  41. Kaas JH, Merzenich MM, Killackey HP. The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. Annu Rev Neurosci1983;6:325–56.[ISI][Medline]
  42. Valeriani M, Restuccia D, DiLazzaro V, Franceschi F, Fabbriciani C, Tonali P. Central nervous system modifications in patients with lesion of the anterior cruciate ligament of the knee. Brain1996;119:1751–62.[Abstract]
  43. Johansson H, Sjölander P, Sojka P, Wadell I. Reflex actions on the gamma-muscle-spindle system of muscles acting at the knee joint elicited by stretch of the posterior cruciate ligament. Neuro-Orthopedics1989;8:9–21.
Submitted 9 June 1999; revised version accepted 28 January 2000.



This Article
Abstract
Full Text (PDF)
Alert me when this article is cited
Alert me if a correction is posted
Services
Email this article to a friend
Similar articles in this journal
Similar articles in ISI Web of Science
Similar articles in PubMed
Alert me to new issues of the journal
Add to My Personal Archive
Download to citation manager
Search for citing articles in:
ISI Web of Science (6)
Disclaimer
Request Permissions
Google Scholar
Articles by Weiler, H.-T.
Articles by Awiszus, F.
PubMed
PubMed Citation
Articles by Weiler, H.-T.
Articles by Awiszus, F.