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SCIENTIFIC ARTICLE Evidence of Wrist Proprioceptive Reflexes Elicited After Stimulation of the Scapholunate Interosseous Ligament Elisabet Hagert, MD, PhD, Jonas K. E. Persson, MD, PhD, Michael Werner, MD, Björn-Ove Ljung, MD, PhD Purpose Recent publications on the sensory innervation of wrist ligaments have challenged our understanding of ligaments as mere passive restraints in wrist stability. Mechanoreceptors in ligaments have a role in signaling joint perturbations, in which the afferent information is believed to influence periarticular muscles. The scapholunate interosseous ligament is one of the most richly innervated ligaments in the wrist. The purpose of our study was to investigate the possible existence of a wrist proprioceptive reflex, by which afferent information elicited in the scapholunate interosseous ligament was hypothesized to influence the muscles moving the wrist joint. Methods Nine volunteers (4 women and 5 men; mean age, 26 years; range, 21–28 years) participated in this study. Using ultrasound guidance, a fine-wire electrode was inserted into the dorsal scapholunate interosseous ligament and stimulated with four 1-ms pulses at 200 Hz. Electromyographic activities in extensor carpi radialis brevis, extensor carpi ulnaris, flexor carpi radialis, and flexor carpi ulnaris muscles were recorded using surface electrodes with the wrist actively positioned in isometric extension, flexion, and radial and ulnar deviation. The average EMGs from 30 consecutive stimulations were rectified and analyzed using the Student’s t-test to compare the prestimulus (t1) and poststimulus (t2) EMG activities. Results Statistically significant changes in poststimulus EMG activity (t1– t2) were observed at various time intervals. Within 20 ms, an excitation was seen in the flexor carpi radialis and flexor carpi ulnaris in extension, radial and ulnar deviation, and in extensor carpi radialis brevis in flexion. Co-contractions between agonist and antagonist muscles were observed, with peaks around 150 ms after stimulus. Conclusions We present evidence of wrist ligamento-muscular reactions. The early-onset reactions may serve in a joint-protective manner, and later co-contractions indicate a supraspinal control of wrist neuromuscular stability. These findings contribute new information to the physiologic functions of the wrist joint, which may further our understanding of dynamic wrist stability and serve as a foundation for future studies on proprioceptive dysfunctions after wrist ligament injuries. (J Hand Surg 2009;34A:642–651. Copyright © 2009 by the American Society for Surgery of the Hand. All rights reserved.) Key words Ligament, ligamento-muscular, neuromuscular, proprioception, wrist. From the Karolinska Institute, Department of Clinical Science and Education, Section of Hand Surgery, Södersjukhuset, Stockholm, Sweden; Karolinska Institute, Department of Clinical Neuroscience, Section of Neurophysiology, Stockholm, Sweden; Department of Radiology, Södersjukhuset, Stockholm, Sweden; and University of Gothenburg, Sahlgrenska Academy, Institute of Clinical Sciences, Department of Hand Surgery, Göteborg, Sweden. Received for publication September 11, 2008; accepted in revised form December 2, 2008. The authors wish to express their sincere gratitude to Hans Pettersson, PhD, institute statistician at Karolinska Institute, Department of Clinical Science and Education, Södersjukhuset, for his invaluable advice in the statistical analysis of this material. We also wish to thank radiology nurse Tina Norström for her superb practical assistance in the ultrasound laboratory. 642 䉬 ©  ASSH 䉬 Published by Elsevier, Inc. All rights reserved. Supported by Karolinska Institute and by the Department of Hand Surgery, Södersjukhuset, Stockholm, Sweden. No benefits in any form have been received or will be received related directly or indirectly to the subject of this article. Corresponding author: Elisabet Hagert, MD, PhD, Karolinska Institute, Department of Hand Surgery, Södersjukhuset, 118 83 Stockholm, Sweden; e-mail: elisabet.hagert@ki.se. 0363-5023/09/34A04-0007$36.00/0 doi:10.1016/j.jhsa.2008.12.001 EVIDENCE OF WRIST PROPRIOCEPTIVE REFLEXES T of the wrist joint, an equilibrium of both static and dynamic functions must be maintained. Whereas static stability is determined by the articular congruency and ligamentous restraints of the wrist, dynamic stability is determined by the neuromuscular and proprioceptive influences on the wrist joint.1 The term proprioception was first described by Sir Charles Scott Sherrington in 1906 as sensations arising in the deep areas of the body, contributing to conscious sensations, postural equilibrium, and joint stability.2 Since then, the field of proprioceptive research has come to entail any and all of these sensory modalities. To promote the research field concerning joint stability, a more precise terminology, sensorimotor function,3 has been advocated. This term implies the total integration of sensory, motor, and central functions in processes pertaining to joint homeostasis. Our understanding of the role of ligaments in joint stability has evolved during the past century from that of passively stabilizing to sensory dynamic structures.4,5 Whereas thorough research into the innervation of ligaments and their contributions to joint equilibrium has been performed on the knee, ankle, spine, shoulder, and elbow joints,4,6 –9 the sensorimotor functions of the wrist are still largely unknown. Recent investigations have mapped the mechanoreceptor populations in wrist ligaments, and distinct variations with regard to receptor density and ligament structure were found, signifying differential roles in functional joint stability.10,11 One of the richest innervated ligaments is the scapholunate interosseous ligament, which is recognized as a key structure for maintaining carpal stability.12 The dorsal region of the scapholunate interosseous ligament, in particular, has properties enabling the resistance of extreme loads,13 as well as an abundance of sensory nerve endings.10,14 Because the scapholunate interosseous ligament is consistently regarded as a biomechanically important ligament, as well as recognized as a richly innervated ligament, we hypothesized that it has a role in the proprioceptive control of the wrist. The purpose of our study was to investigate the possible existence of wrist ligamento-muscular reflexes, in which sensory information from the scapholunate interosseous ligament is assumed to influence the forearm muscles associated with wrist motion. O ACHIEVE STABILITY MATERIALS AND METHODS Subjects The design of this study was approved by the regional ethical review board. Nine healthy volunteers, 4 women 643 and 5 men (mean age, 26 years; range, 21–28 years) were included, and all subjects gave informed consent to participate in the study. The participants were all healthy, with no reported history of wrist trauma and no clinical signs of wrist dysfunction upon examination by a specialist hand surgeon. The dominant hand was examined in all subjects. Ultrasound techniques An Acuson Sequoia 512 (Siemens Medical Solutions Inc., Malvern, PA) with a transverse 8-MHz transducer was used. A fine, stainless steel wire electrode (model 1512A-M; Life-Tech Inc., Stafford, TX) with a distal, uninsulated hook was preinserted in a 0.5-mm puncture needle. Using sterile conditions, we identified the dorsal scapholunate interosseous ligament in a transverse-dorsal view between the dorsal surfaces of the scaphoid and lunate, as previously described,15,16 and the puncture needle subsequently advanced into the ligament. As the needle was retracted, the hook of the electrode remained fixed in the dorsal scapholunate interosseous ligament. Ultrasound imaging confirming correct needle position was obtained from all subjects (Fig. 1). Ultrasound was additionally used to identify the extensor carpi radialis brevis (ECRB), extensor carpi ulnaris (ECU), flexor carpi radialis (FCR), and flexor carpi ulnaris (FCU) muscles. The EMG surface electrodes were correctly positioned according to Perotto and Delagi17 at the center of each muscle belly. EMG recordings EMG signals were recorded by Ag-AgCl surface electrodes (NE-113A; Nihon Kohden Co., Tokyo, Japan; diameter, 10 mm; interelectrode distance, 20 mm). The reference electrode was placed on the dorsum of the hand, just distally to the insertion point of the stimulating electrode located in the ligament. The ground surface electrode (Rec. No. 019-4009100; Nicolet Biomedical, Madison, WI) was placed between the stimulating and the surface electrodes, which were then connected to a 4-channel EMG (KeyPoint, v5.09; Medtronic, Copenhagen, Denmark). Visual monitoring of EMG signals on the oscilloscope while the subject voluntarily contracted each respective forearm muscle was used to check the accuracy of electrode placement. Experimental protocol The subject was seated in an examination chair with the arm placed in an armrest. The position of the arm was 20° shoulder abduction, 80° elbow flexion, and pronated forearm. During the experiment, the wrist was actively positioned in an average of 40° wrist extension, JHS 䉬 Vol A, April  644 EVIDENCE OF WRIST PROPRIOCEPTIVE REFLEXES FIGURE 1: A A transverse-dorsal ultrasound image of the dorsal surfaces of the scaphoid (SCA) and lunate (LUN). The inserted needle point is visualized (arrows) in the scapholunate interval, positioned in the dorsal region of the scapholunate interosseous ligament. B Same image colorized to facilitate the visualization of the scaphoid (blue), lunate (green), and dorsal scapholunate interosseous ligament (purple). The needle point is graphically illustrated in the ligament (blue arrow). 20° flexion, 20° radial deviation, and 30° ulnar deviation, respectively. The subject performed isometric contraction, using submaximal force, in each wrist position, while the motion was resisted manually by one of the examiners. The electrical stimulus consisted of four 1-ms pulses delivered at 200 Hz by the fine-wire electrode placed in the ligament. The individual threshold for consciously sensing the stimulus was determined and the test stimulus set at 2 to 3 times this sensory threshold (mean, 2.0 mA; range, 1.2–5.0 mA) yet consistently below the nociceptive threshold. The scapholunate interosseous ligament was subsequently stimulated with 30 consecutive stimulations at 2-second intervals. The raw EMG signals were amplified, band-pass filtered, and digitally sampled from 100 ms before to 700 ms after the stimulus. As an internal control, stimulation of the dorsal scapholunate interosseous ligament was performed while the forearm muscles were relaxed, which resulted in no reflex reactivity in the ECRB, ECU, FCR, and FCU muscles. Additionally, to rule out stimulation of nerve endings in the skin, 2 mL lidocaine hydrochloride was infiltrated intradermally around the stimulating electrode in 2 subjects and the experiment was subsequently repeated, which resulted in no change in reflex reactivity. MA). After rectification, each subject and all 4 muscles were analyzed independently in each separate wrist position. The root mean square was subsequently used for statistical analysis using the Student’s t-test (2tailed, for independent variables). Poststimulus changes in EMG activity (recorded as changes in EMG amplitude) that were statistically significant (p ⬍ .05) in a majority of subjects (5 or more) were noted as peaks of EMG activity. These peaks were subsequently plotted in poststimulus time histograms. The statistical models were chosen in collaboration with the institute statistician. RESULTS General observations Patterns of muscle reactivity resembling varying recruitment orders of the forearm muscles were observed at various time intervals after electrical stimulation of the scapholunate interosseous ligament. The median values of all statistically significant changes (p ⬍ .05) in amplitude (t1 – t2) are plotted in poststimulus time histograms (Figs. 2– 6), which depict the sequence of events occurring in each wrist position. The time-related changes in amplitude may be divided into the following reaction patterns: 1. Immediate reaction. The primary muscle response, Statistical analysis The average EMG data from the 30 consecutive trials were exported to and mounted in a software program (Microsoft Excel 2004, v.11.3.7; Microsoft Corp., Redmond, WA). The EMG data were divided into time intervals, for which the prestimulus 100-ms interval was regarded as baseline (t1), and the poststimulus EMG (t2) was divided into 20-ms intervals, up to 500 ms after stimulation. The EMG spreadsheets were imported into software (OriginPro v.7.5714; Origin Lab Corp., Northampton, which is observed within the first 20-ms interval after stimulation of the ligament. This reaction was of a monophasic type and presented in the antagonist muscles, as related to each wrist position. 2. Reciprocal activation. The immediate reaction was frequently followed by a corresponding activation in the agonist muscle(s) for each wrist position, from around 20 to 60 ms after stimulation, with or without concurrent antagonist activation. 3. Co-contraction. An excitatory reaction occurring in 2 or more of the recorded forearm muscles, JHS 䉬 Vol A, April  EVIDENCE OF WRIST PROPRIOCEPTIVE REFLEXES FIGURE 2: EMG amplitude (y axis) in all forearm muscles along a time line (x axis), depicting the simultaneous muscle activity in the ECRB, ECU, FCR, and FCU muscles after stimulation of the ligament with the wrist in isometric extension. Positive values indicate an increase in muscle amplitude, an excitation, whereas negative values denote a decrease in amplitude, an inhibition, compared with the prestimulus median value (baseline, t1). Note the peaks of co-contraction that occur around 50, 150, and 250 ms. indicating a simultaneous contraction of both agonist and antagonist muscles. This intermediate reaction generally lasted about 100 ms, with peak activity around 150 ms after stimulation. The largest changes in muscle amplitude were noted during this reaction. 4. Receding reactions. From time intervals around 250 –300 to 500 ms after stimulation, the general muscle pattern was one of receding activity. If excitation occurred, the amplitudes were generally smaller than those previously noted. Additionally, inhibition of EMG activity was frequently seen during this interval. Specific patterns in each wrist position Extension: The muscle pattern seen simultaneously in the 4 forearm muscles is illustrated in Figure 2, and the precise change in each muscle is depicted in poststimulus time histograms in Figure 3. The immediate reaction after stimulation with the wrist in extension was observed in the FCR and FCU muscles. This primary reaction was instantly followed by a reciprocal activation of the ECRB and ECU muscles from 20 to 60 ms after stimulus, and, additionally, of the FCR muscle from 40 to 60 ms after stimulation. A longer period of co-contraction occurs in all 4 muscles at time intervals from 60 – 80 to approximately 160 –180 ms. This period of co-contraction contains the largest changes in amplitude seen in the 645 ECRB muscle in extension (median, 42.29 ␮V). A third phase of co-contraction is seen in the ECRB, ECU, and FCU muscles, peaking around 250 ms, during which time the excitatory amplitudes are smaller than the preceding recordings. The final phase is one of receding activity, with inhibitory reactions in the FCR, ECU, and ECRB muscles. Figure 7 depicts the actual rectified EMG in extension from 1 subject and illustrates the co-contraction patterns described above. Flexion: The immediate poststimulus reaction in flexion was observed in the ECRB muscle (Fig. 4). After this initial reaction, only intermittent reactions were seen in the ECRB and ECU muscles. A subsequent reciprocal activation in the FCR and FCU muscles was noted from 20 to 60 ms. This reaction pattern was again repeated from 120 to 200 ms and contained the largest changes in amplitude observed in the FCU muscle (median, 9.76 ␮V). Only a brief period of co-contraction is observed in the ECU and FCR muscles, occurring at 240 to 260 ms. The receding activity, approximately 320 ms after stimulus, is characterized by inhibitory reactions in the FCR and FCU muscles, followed by sporadic excitatory responses in the FCR muscle. Radial deviation: The immediate reaction is observed in the FCR and FCU muscles during the initial 20 ms (Fig. 5). In this position, the largest changes in immediate amplitude in the FCR and FCU muscles were observed (median, 8.12 and 5.82 ␮V, respectively). This is directly followed by a co-contraction in the ECRB, ECU, and FCR muscles from 20 to 60 ms. A phase of co-contraction is once again seen approximately 100 to 160 ms after stimulus, with excitation of all wrist muscles. As in the extended wrist position, this phase contains the largest amplitude changes in the ECRB muscle (median, 7.47 ␮V). In the final phase of receding activity, co-contraction with smaller amplitudes is seen in the ECRB and FCR muscles around 250 ms, followed by inhibitory reactions in the ECRB and ECU muscles and excitatory reactions in the FCR muscle. Ulnar deviation: As in the other wrist positions, an immediate reaction is seen, occurring in the FCR and FCU muscles (Fig. 6). In general, however, the reaction pattern observed in ulnar deviation differs greatly from that of the other positions. No periods of co-contraction were observed, and only sporadic excitatory responses in the FCR and ECRB muscles occurred. In fact, the predominant muscular response JHS 䉬 Vol A, April  646 EVIDENCE OF WRIST PROPRIOCEPTIVE REFLEXES FIGURE 3: Poststimulus time histograms of the significant (p ⬍ .05) changes in amplitude (t1 – t2) observed after stimulation (stim) of the scapholunate interosseous ligament with the wrist in a position of isometric extension. Each column represents the statistically significant (p ⬍ .05) median value for a specific time interval. From top to bottom: ECRB, ECU, FCR, and FCU muscles. Note the early reaction in FCR and FCU muscles. The largest excitation is seen in the primary motor, ECRB muscle, around 150 ms. is one of inhibition of the primary motor in ulnar deviation—the ECU muscle. A total of 5 inhibitory phases are seen between 80 and 420 ms after stimulus. DISCUSSION In this study, we have used a protocol of electrical stimulation of the scapholunate interosseous ligament while monitoring the EMG activities in 4 forearm muscles to investigate possible wrist ligamento-muscular connections. Our experimental procedure was based on previously published reports on ligamento-muscular reflexes in the shoulder and knee joints.8,18,19 We have been able to confirm our hypothesis and, for the first time, present evidence of reactions between a wrist ligament (scapholunate interosseous ligament) and 4 muscles responsible for wrist motion (ECRB, ECU, FCR, and FCU). Furthermore, these ligamentomuscular reflexes exhibit linear reaction patterns, suggesting time-dependent recruitment phases of the forearm muscles. In the subsequent sections, we will discuss the possible role of these recruitment phases in wrist neuromuscular stability. Immediate muscle reactions The findings of mechanoreceptor populations in ligaments have elicited hypotheses regarding the sensory role of ligaments in providing reflex stability in the event of joint perturbations. These concepts of jointprotective reflexes were first studied by Palmer in 195820 and have subsequently been confirmed in the knee, ankle, shoulder, and elbow joints.4,5,9,21 Controversy exists regarding protective reflexes because the efficacy of a defensive reflex is entirely dependent on the immediacy of the ligamento-muscular reaction. Hence, to be joint protective, an adequate reaction would need to be equivalent in response time to a monosynaptic stretch reflex (ie, patellar reflex), when the antagonist muscles act as first line of defense to break a potentially damaging joint motion. Recordings from the receptive fields of mechanoreceptors in human glabrous skin have shown that these nerve endings belong to the fastest group of nerve fibers, group I, or the A␣-fiber.22 In the joint, however, mechanoreceptors are believed to belong to group II, or A␤-afferents, with conduction velocities of approximately 70 m/s.23 Additional investigations of these nerve conduction velocities in the human forearm have confirmed compound nerve velocity rates indicative of fast-reacting and proprioceptive afferents.24,25 Furthermore, experiments on the excitation of human flexor motoneurons have shown that stimulation of the median and/or ulnar nerves at the level of the wrist JHS 䉬 Vol A, April  EVIDENCE OF WRIST PROPRIOCEPTIVE REFLEXES 647 FIGURE 4: Poststimulus time histograms of the significant (p ⬍ .05) changes in amplitude (t1 – t2) observed after stimulation (stim) of the scapholunate interosseous ligament with the wrist in a position of isometric flexion. From top to bottom: ECRB, ECU, FCR, and FCU muscles. The early-onset reaction is observed in the ECRB muscle. The predominant activity is observed in the wrist flexors, the FCR and FCU muscles, with the largest excitation in the primary motor, FCU muscle, around 150 ms. Only a brief period of co-contraction is seen around 250 ms. joint elicits monosynaptic excitations of the FCR and FCU muscles, occurring within 20 ms after stimulation.26,27 These reaction times are similar to the immediate reactions observed in our study, indicating that these, too, may be of monosynaptic origin. In our study, a monophasic immediate reflex was present in all wrist positions within the first 20 ms after stimulation of the ligament. In extension and in radial and ulnar deviation, this first response was seen in the FCR and FCU muscles. In these 3 wrist positions, the dorsal scapholunate interosseous ligament is in a state of elongation,28 leaving the ligament vulnerable to disruption. The simultaneous contraction of FCR and FCU muscles as paired antagonists would counteract a potentially noxious extension or deviation motion. Similarly, with the wrist in a flexed position, the immediate response was seen in the primary antagonist, the ECRB muscle. The short-onset latency and the specific recruitment of muscle groups to disrupt potentially damaging wrist positions may indicate that the immediate reactions recorded in our study serve in a joint-protective manner. The precise afferent pathways of these early reflexes, however, are not delineated in our study. Based on previous publications, we speculate that these reactions are of a monosynaptic spinal origin6 or, pos- sibly, modulations of ongoing muscle activity through local gamma-fusimotor systems.4 Co-contraction After the immediate reflex, a pattern of coactivation of agonist and antagonist muscles, co-contraction, was observed. These reactions generally commenced around 50 ms after stimulation, with peak amplitudes of EMG activity around 150 ms, the largest amplitudes being observed in the dominant muscle for each wrist position. The later-onset latency of these reactions suggest that they differ from the immediate responses described above. Although we currently lack information on the precise path of proprioceptive information from the wrist joint, studies of cortical somatosensory evoked potentials from the median and radial nerves29 and of the effects of transcranial magnetic stimulation on reflexes in the forearm muscles30 indicate afferent and efferent time intervals to correspond with these periods of coactivation. This intermediate reaction pattern is most likely the result of a polysynaptic spinal reflex arc influenced by supraspinal pathways.31 The long-onset latency of the co-contraction reaction suggests that it has importance in the long-term control of joint neuromuscular stability as opposed to the sim- JHS 䉬 Vol A, April  648 EVIDENCE OF WRIST PROPRIOCEPTIVE REFLEXES FIGURE 5: Poststimulus time histograms of the significant (p ⬍ .05) changes in amplitude (t1 – t2) observed after stimulation (stim) of the scapholunate interosseous ligament with the wrist in a position of isometric radial deviation. From top to bottom: ECRB, ECU, FCR, and FCU muscles. Note the early reactions in the FCR and FCU muscles. The largest excitations are seen in the FCR muscle within the first 20 ms, and in ECRB muscle around 150 ms. Peaks of co-contraction are observed around 50, 150, and 250 ms. ple joint-protective reflex described above. Co-contraction has previously been seen as an effective method of stability in the knee joint, where perturbation of the anterior cruciate ligament has elicited reflex actions in both hamstring and quadriceps musculature.32,33 Global contraction of agonist and antagonist muscles around a joint will result in general joint stiffness, effectively reducing the risk of joint damage.34 Studies of the biomechanical adaptations of the wrist have shown a substantial increase in co-contraction after unstable loading of the wrist,35 as well as a dynamic ability to adapt these co-contractions to variations in destabilizing actions.36 Muscles that are preactivated have a general stiffness at the onset of joint perturbations, and thus will respond more quickly and with greater amplitudes.3 This corresponds with our observations that the largest excitatory changes in amplitude are seen in the agonist muscles (ECRB in extension and radial deviation, FCU in flexion) during the intermediate period of co-contraction. The functional implication of co-contraction is not merely one of joint stability after external loads. More importantly, the delicate balance of co-contraction is believed to be important in maintaining smooth joint motions. This ability to sustain an adequate joint equilibrium has been shown to be impaired in anterior cruciate ligament– deficient knees,37 where an inade- quate neuromuscular recruitment renders changes in knee kinematics potentially harmful to the joint.38 Whether similar disturbances occur in wrist proprioceptive functions after ligament injuries is currently unknown. Inhibition Although co-contraction is an effective strategy to increase joint stiffness and maintain neuromuscular joint stability, it is correlated with a large expenditure of energy.36 Additionally, a prolonged loading of ligaments has been associated with an increase of reflex thresholds and a reciprocal decrease in EMG activity.5 These combined observations may in part explain the receding EMG activity observed during the final stages of our experiments. This period of general fatigue is paradoxically a phase in which the efforts to maintain joint stability may result in a joint susceptible to damage and unable to adequately respond to external forces. Clinical relevance The findings of specific ligamento-muscular reflexes elicited from electrical stimulation of the scapholunate interosseous ligament confirm our hypothesis that this ligament has a sensory and proprioceptive function. The consequence of our findings is the realization that a JHS 䉬 Vol A, April  EVIDENCE OF WRIST PROPRIOCEPTIVE REFLEXES 649 FIGURE 6: Poststimulus time histograms of the significant (p ⬍ .05) changes in amplitude (t1 – t2) observed after stimulation (stim) of the scapholunate interosseous ligament with the wrist in a position of isometric ulnar deviation. From top to bottom: ECRB, ECU, FCR, and FCU muscles. The earliest reactions are seen in the FCR and FCU muscles. No periods of co-contraction are observed, and the predominant activity is one of inhibition in the ECU muscle, where a total of 5 inhibitory phases are seen from 80 to 420 ms. scapholunate interosseous ligament injury entails a loss of both structural and sensory function in the carpus. Additionally, the reflexes found indicate both a simple joint-protective purpose and a refined muscle control of the wrist. By analyzing these patterns of neuromuscular stability and co-contraction further, we hope to enhance our understanding of the long-term effects of wrist ligament injuries and generate adequate neuromuscular rehabilitation techniques to promote proprioception reeducation. The scapholunate interosseous ligament, however, is only one of several richly innervated wrist ligaments. We still lack substantial information regarding ligamento-muscular control from other parts of the carpus and distal radioulnar joint, which must be obtained before we truly can understand the complex mechanisms of wrist sensorimotor functions. Assumptions and limitations Although elicitation of ligament reflexes through electrical stimulation is an accepted methodology in proprioception research, the technique has several limitations.39 The primary concern is the assumption that the electrical discharge will, in some manner, correspond with a physiologic joint perturbation. This is unknown, leaving us with the possibility that the reactions ob- served are artificial. In our protocol, the scapholunate interosseous ligament was stimulated at intensities 2 to 3 times the sensory, but below the nociceptive, threshold. None of our subjects reported pain during application of the electrical stimuli, indicating that no A⭸- or C-fibers were stimulated. Because fine afferents require high levels of stimulation to elicit a nociceptive response,40 we believe our low-intensity stimulus was within an acceptable physiologic range to elicit responses from mechanoreceptive A␤-afferents. The second concern is the position of the electrode. Because our aim was to study reflexes elicited in the scapholunate interosseous ligament, a displacement of the electrode may cause an actual stimulation of receptors in the skin and/or dorsal wrist capsule. To eliminate the possibility of cutaneous contributions, the skin around the stimulating fine-wire electrode was anesthetized in 2 of our subjects after completion of the first experiment. After the skin was desensitized, a second series of stimulations of the dorsal scapholunate interosseous ligament was performed. Skin desensitization did not alter the muscular reactions, which led us to believe that the reactions observed were indeed elicited from the ligament itself. The dorsal capsule, however, cannot be desensitized without risk of influencing the afferent information from the dorsal scapholunate in- JHS 䉬 Vol A, April  650 EVIDENCE OF WRIST PROPRIOCEPTIVE REFLEXES FIGURE 7: Rectified EMG (averaged data from 30 consecutive stimulations) from 1 subject, with the wrist in isometric extension. From top to bottom: A ECRB, B ECU, C FCR, and D FCU muscles. The baseline (horizontal line) depicts the prestimulus root mean square value of each muscle. The stimulation artifacts are clearly seen in FCR and FCU muscles. The onset of cocontraction (dotted vertical line) is observed in all 4 muscles around 50 ms after stimulation of the scapholunate interosseous ligament. terosseous ligament. Furthermore, it cannot be identified using sonographic techniques, which eliminated the possibility of inserting a capsular stimulating electrode to evaluate possible reflex reactions. The dorsal wrist capsule, innervated by terminal branches from the posterior interosseous, dorsal radial and ulnar sensory nerves,41 has not been studied with regard to presence of proprioceptive nerve endings. Hence, we currently lack information on its possible role in wrist proprioception. Finally, the number of subjects included in this study was small, thus limiting the statistical merit of our findings. The experimental setup is considered invasive, and institutional review board approval was confined to a descriptive study. In comparison with previously published experiments on joint ligamento-muscular reflexes,8,18,42 our study is one of the largest series conducted on human subjects. REFERENCES 1. Linscheid RL, Dobyns JH. Dynamic carpal stability. Keio J Med 2002;51:140 –147. 2. Sherrington CS. The integrative action of the nervous system. New Haven, CT: Yale University Press, 1906:50. 3. Lephart SM, Riemann BL, Fu FH. Introduction to the sensorimotor system. In: Lephart SM, Fu FH, eds. Proprioception and neuromuscular control in joint stability. Champaign, IL: Human Kinetics, 2000:xvii–xxiv. 4. Johansson H, Sjolander P, Sojka P. A sensory role for the cruciate ligaments. Clin Orthop 1991;268:161–178. 5. Solomonow M. Sensory-motor control of ligaments and associated neuromuscular disorders. J Electromyogr Kinesiol 2006;16:549–567. 6. Solomonow M, Krogsgaard M. Sensorimotor control of knee stability. A review. Scand J Med Sci Sports 2001;11:64 – 80. 7. Konradsen L. Sensori-motor control of the uninjured and injured human ankle. J Electromyogr Kinesiol 2002;12:199 –203. 8. Diederichsen LP, Norregaard J, Krogsgaard M, Fischer-Rasmussen T, Dyhre-Poulsen P. Reflexes in the shoulder muscles elicited from the human coracoacromial ligament. J Orthop Res 2004;22:976–983. 9. Phillips D, Petrie S, Solomonow M, Zhou BH, Guanche C, D’Ambrosia R. Ligamentomuscular protective reflex in the elbow. J Hand Surg 1997;22A:473– 478. 10. Hagert E, Garcia-Elias M, Forsgren S, Ljung BO. Immunohistochemical analysis of wrist ligament innervation in relation to their structural composition. J Hand Surg 2007;32A:30 –36. 11. Hagert E, Forsgren S, Ljung BO. Differences in the presence of mechanoreceptors and nerve structures between wrist ligaments may imply differential roles in wrist stabilization. J Orthop Res 2005;23: 757–763. 12. Short WH, Werner FW, Green JK, Sutton LG, Brutus JP. Biome- JHS 䉬 Vol A, April  EVIDENCE OF WRIST PROPRIOCEPTIVE REFLEXES 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. chanical evaluation of the ligamentous stabilizers of the scaphoid and lunate: part III. J Hand Surg 2007;32A:297–309. Berger RA, Imeada T, Berglund L, An KN. Constraint and material properties of the subregions of the scapholunate interosseous ligament. J Hand Surg 1999;24A:953–962. Hagert E, Ljung BO, Forsgren S. General innervation pattern and sensory corpuscles in the scapholunate interosseous ligament. Cells Tissues Organs 2004;177:47–54. Finlay K, Lee R, Friedman L. Ultrasound of intrinsic wrist ligament and triangular fibrocartilage injuries. Skeletal Radiol 2004;33:85–90. Jacobson JA, Oh E, Propeck T, Jebson PJ, Jamadar DA, Hayes CW. Sonography of the scapholunate ligament in four cadaveric wrists: correlation with MR arthrography and anatomy. AJR Am J Roentgenol 2002;179:523–527. Perotto A, Delagi EF. Anatomical guide for the electromyographer: the limbs and trunk. 4th ed. Springfield, IL: Charles C. Thomas, 2005:38 –56. Dyhre-Poulsen P, Krogsgaard MR. Muscular reflexes elicited by electrical stimulation of the anterior cruciate ligament in humans. J Appl Physiol 2000;89:2191–2195. Tsuda E, Okamura Y, Otsuka H, Komatsu T, Tokuya S. Direct evidence of the anterior cruciate ligament-hamstring reflex arc in humans. Am J Sports Med 2001;29:83– 87. Palmer I. Pathophysiology of the medial ligament of the knee joint. Acta Chir Scand 1958;115:312–318. Voigt M, Jakobsen J, Sinkjaer T. Non-noxious stimulation of the glenohumeral joint capsule elicits strong inhibition of active shoulder muscles in conscious human subjects. Neurosci Lett 1998;254: 105–108. Vallbo AB, Hagbarth KE, Torebjork HE, Wallin BG. Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. Physiol Rev 1979;59:919 –957. Gilman S. Joint position sense and vibration sense: anatomical organisation and assessment. J Neurol Neurosurg Psychiatry 2002; 73:473– 477. Tran TD, Lam K, Hoshiyama M, Kakigi R. A new method for measuring the conduction velocities of Abeta-, Adelta- and C-fibers following electric and CO(2) laser stimulation in humans. Neurosci Lett 2001;301:187–190. Metso AJ, Palmu K, Partanen JV. Compound nerve conduction velocity—a reflection of proprioceptive afferents? Clin Neurophysiol 2008;119:29 –32. Malmgren K, Pierrot-Deseilligny E. Evidence for non-monosynaptic Ia excitation of human wrist flexor motoneurones, possibly via propriospinal neurones. J Physiol 1988;405:747–764. Lourenco G, Iglesias C, Marchand-Pauvert V. Effects produced in human arm and forearm motoneurons after electrical stimulation of 28. 29. 30. 31. 32. 33. 34. 35. 36. 37. 38. 39. 40. 41. 42. 651 ulnar and median nerves at wrist level. Exp Brain Res 2007;178:267–284. Upal MA, Crisco JJ, Moore DC, Sonenblum SE, Wolfe SW. In vivo elongation of the palmar and dorsal scapholunate interosseous ligament. J Hand Surg 2006;31A:1326 –1332. Treede RD, Kunde V. Middle-latency somatosensory evoked potentials after stimulation of the radial and median nerves: component structure and scalp topography. J Clin Neurophysiol 1995;12:291–301. Deuschl G, Michels R, Berardelli A, Schenck E, Inghilleri M, Lücking CH. Effects of electric and magnetic transcranial stimulation on long latency reflexes. Exp Brain Res 1991;83:403– 410. Wojtys EM, Huston LJ. Neuromuscular performance in normal and anterior cruciate ligament-deficient lower extremities. Am J Sports Med 1994;22:89 –104. Hirokawa S, Solomonow M, Lu Y, Lou ZP, D’Ambrosia R. Anterior-posterior and rotational displacement of the tibia elicited by quadriceps contraction. Am J Sports Med 1992;20:299 –306. MacWilliams BA, Wilson DR, DesJardins JD, Romero J, Chao EY. Hamstrings cocontraction reduces internal rotation, anterior translation, and anterior cruciate ligament load in weight-bearing flexion. J Orthop Res 1999;17:817– 822. Solomonow M. Ligaments: a source of work-related musculoskeletal disorders. J Electromyogr Kinesiol 2004;14:49 – 60. De Serres SJ, Milner TE. Wrist muscle activation patterns and stiffness associated with stable and unstable mechanical loads. Exp Brain Res 1991;86:451– 458. Milner TE. Adaptation to destabilizing dynamics by means of muscle cocontraction. Exp Brain Res 2002;143:406 – 416. Chmielewski TL, Hurd WJ, Snyder-Mackler L. Elucidation of a potentially destabilizing control strategy in ACL deficient non-copers. J Electromyogr Kinesiol 2005;15:83–92. Rudolph KS, Eastlack ME, Axe MJ, Snyder-Mackler L. 1998 Basmajian Student Award Paper: movement patterns after anterior cruciate ligament injury: a comparison of patients who compensate well for the injury and those who require operative stabilization. J Electromyogr Kinesiol 1998;8:349 –362. Riemann BL, Myers JB, Lephart SM. Sensorimotor system measurement techniques. J Athl Train 2002;37:85–98. Grigg P. Properties of sensory neurons innervating synovial joints. Cells Tissues Organs 2001;169:218 –225. Van de Pol GJ, Koudstaal MJ, Schuurman AH, Bleys RL. Innervation of the wrist joint and surgical perspectives of denervation. J Hand Surg 2006;31A:28 –34. Fischer-Rasmussen T, Krogsgaard MR, Jensen DB, Dyhre-Poulsen P. Muscle reflexes during gait elicited by electrical stimulation of the posterior cruciate ligament in humans. J Orthop Res 2002;20:433– 438. JHS 䉬 Vol A, April 