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Relationship between two proprioceptive measures and stiffness at the ankle
Journal of Electromyography and Kinesiology 14 (2004) 317–324 www.elsevier.com/locate/jelekin
Relationship between two proprioceptive measures and stiffness at the ankle Carrie L. Docherty a,∗, Brent L. Arnold b, Steven M. Zinder a, Kevin Granata c, Bruce M. Gansneder a a
Curry School of Education, University of Virginia, 210 Emmet St South, Suite #203, P.O. Box 400407, Charlottesville, VA 22904-4407, USA b School of Education, Virginia Commonwealth University, Richmond, VA, USA c School of Medicine, University of Virginia, Charlottesville, VA, USA Received 8 October 2002; received in revised form 25 February 2003; accepted 27 February 2003
Abstract Previous research has investigated the role of proprioception and stiffness in the control of joint stability. However, to date, no research has been done on the relationship between proprioception and stiffness. Therefore, the purpose of this study was to determine the relationship between force sense, joint reposition sense, and stiffness at the ankle. A heterogeneous sample was obtained for this study; 20 of the 40 participants had a history of ankle sprains, and 13 of the 20 had been diagnosed by a physician (two mild ankle sprains, seven moderate sprains, four severe sprains). All subjects were asymptomatic and active at the time of the study. Active joint reposition sense was measured using a custom-built ankle goniometer, force sense was measured unilaterally and contralaterally with a load cell, and ankle muscle stiffness was measured via transient oscillation using a custom-built inversion– eversion cradle. We found no significant correlations between stiffness and joint reposition sense, with values of r ranging from 0.01 to 0.21. Significant correlations were found between stiffness and force sense. Specifically, contralateral force sense reproduction was significantly correlated to stiffness in the injured or “involved” ankle (r’s ranging from 0.47 to 0.65; Pⱕ0.008). Whether the decreased ability to appropriately sense force (increased error) sends information to the central nervous system to increase muscle stiffness in response to an unexpected loss of stability, or whether these two phenomena function independently and both change concurrently as a result of injury to the system requires further investigation. 2003 Elsevier Ltd. All rights reserved. Keywords: Joint reposition sense; Force sense; Force matching; Joint stability
1. Introduction Loss of stability has been theorized to be a primary cause of joint injury. Joint stability is the ability to maintain or quickly return to proper positioning following a perturbation [1]. Maintenance of joint stability is mediated by the sensorimotor system through a combination of feedforward and feedback controls. The feedforward process prepares the system for the upcoming motor command and receipt of feedback information [2]. Feedback is a continual process of gaining information via the afferent pathways and is primarily regulated from
Corresponding author. Tel.: +1-434-242-7490; fax: +1-434-9241389. E-mail address: [email protected] (C.L. Docherty). ∗
1050-6411/$ - see front matter 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1050-6411(03)00035-X
previous experiences. Both proprioception and muscle stiffness utilize these controls to facilitate proper movement patterns, and more importantly, protect against injury. Proprioception and stiffness both contribute to joint stability, but little research has been conducted to determine if there is a relationship between the two factors. In proprioception, input is received from the peripheral afferents (muscle spindles, joint receptors, cutaneous receptors, and golgi tendon organs (GTOs)) [3], and provides information on limb awareness, position, force, and heaviness. Conscious proprioception senses include kinesthesia, joint position sense, and sense of force [1,4]. Considerable research has been done to explain how injuries affect these proprioceptive capabilities [5–9]. In 1965, Freeman [10] hypothesized that partial de-afferentiation occurs following an ankle injury and leads to
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proprioceptive deficits. This deficit has been confirmed by multiple studies that link functional instability to deficits in proprioceptive capabilities of the ankle [5–9]. While kinesthesia and joint reposition sense have been continually used to assess proprioceptive function at the ankle, force sense has received little attention. Force sense, or sense of heaviness, was one of the earliest methods used to assess peripheral and central control of joint movement dating back to 1834, but modern researchers have failed to further develop this theory at the ankle. Force sensation is defined as the ability to perceive a given force during a voluntary contraction. Testing can be done with unilateral reproduction, contralateral reproduction, or simultaneous reproduction [11]. To date, the majority of force sense research has been done in the upper extremity [12,13]. Only recently has force sense been examined at the ankle, with the purpose of re-establishing this procedure. Using unilateral reproduction, trial reliability was assessed at 50% and 75% maximal voluntary isometric contraction (MVIC). All testing was done in normal, uninjured subjects. Trial reliability was found to be high, with r’s ranging from 0.82–0.89 [14]. The central nervous system receives proprioceptive feedback from the joint via afferent pathways, the same paths used to determine appropriate levels of muscle stiffness [15–18]. Muscle stiffness is the combination of active and passive stiffness, defined as the ratio of change in force to change in length [15]. Active muscle stiffness can be further broken down into intrinsic and reflex stiffness [19]. Intrinsic muscle stiffness provides the first line of defense following a perturbation and is contingent on the level of muscle activation, or the number of actin and myosin bonds, at the time of the perturbation [20–22]. Reflexes have also been shown to increase muscle stiffness, but due to timing issues, the reflexes do not occur quickly enough to protect certain joints against injury [16,17]. However, the reflexes do play an important role in preprogramming the stiffness via the afferent information from previous perturbations [15]. Research has shown that stiffness can protect the joint through limiting excessive joint translations and subsequent ligament strain caused by an external perturbation [23–26]. Muscle spindle afferents play a large role in regulating both muscle stiffness and position and movement sense [27], yet the relationship between proprioception and muscle stiffness is poorly understood. We hypothesized that inappropriate function of the afferent pathways would adversely affect accurate awareness of length and/or tension in the musculotendinous structure and muscle stiffness. Therefore, the purpose of this paper was to evaluate the relationship between force sense, joint reposition sense and stiffness at the ankle joint.
2. Methods 2.1. Subjects Forty healthy college students (11 males, 29 females, 23.2 ± 5.0 years; 168.4 ± 8.6 cm; 68.5 ± 12.1 kg) from a large university volunteered for this study. Each subject completed an orthopedic questionnaire prior to beginning the study. The information obtained from this questionnaire assisted in assuring that a heterogeneous sample was obtained for this study; 20 had a history of ankle sprains to one ankle, 13 of the 20 had been diagnosed by a physician (two mild ankle sprains, seven moderate sprains, four severe sprains), and 18 of the 20 had a history of giving way episodes. All subjects were asymptomatic and active at the time of the study. The University’s Human Investigation Committee approved the study, and all subjects read and signed a written informed consent form prior to beginning testing. 2.2. Test procedures Each subject came to the sports medicine research laboratory on three occasions. During the initial session, the subjects completed the orthopedic questionnaire, MVIC testing, and active joint reposition sense testing. On the second occasion, the subjects performed the force matching protocol, and on the third day, ankle stiffness was measured. All testing was done bilaterally for each of the test conditions. 2.2.1. Maximal voluntary isometric contraction All subjects were barefoot during the testing procedures, and peak force was measured to the nearest 0.1 N. Maximal eversion strength was tested in both ankles. For this procedure, a load cell (Sensotec, Columbus, OH) with a digital readout was mounted to the wall. The subject was positioned supine on a treatment table with the knees flexed to approximately 10°. The thighs were also fixed to minimize involvement of the quadriceps, hamstrings, and gluteus muscles. The foot was placed off the end of the table and attached to the load cell with Velcro straps (Fig. 1). The subject was instructed to maximally evert the foot for 5 sec. This was repeated for three trials, with a 10-sec rest between trials. The average of the three peak isometric values were recorded as the subject’s MVIC. 2.2.2. Joint reposition sense testing Joint reposition sense measurements were taken with a custom-designed electric goniometer [28]. The device was blocked so only inversion and eversion motion could be performed. All subjects were barefoot during the testing and the foot was placed in a heel cup that was directly mounted to the footplate. The lower leg was supported in the leg rest in full extension and both the
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point in the range of motion. The subject was instructed to actively move the foot until the footplate hit the block. Once in the test position, subjects were told to concentrate on the position for 15 sec. The block was then removed, and the subjects were instructed to move the foot to the opposite extreme of motion and then back to the test position. The reference and reproduction angle measurement were recorded from the electronic readout to the nearest tenth of a degree (0.1°). This procedure was repeated for three trials at each test angle with each ankle.
Fig. 1.
Subject positioning for MVIC and force sense procedures.
leg and foot were fastened in position (Fig. 2). The footplate was positioned to place the ankle in subtalar joint neutral (STJN), and the goniometer was set at zero. The subjects closed their eyes throughout the remainder of testing to eliminate any visual cues. All subjects were tested at 20° from STJN for inversion and at 10° from STJN for eversion. Initially, the subjects were asked to move the foot into the extremes of the range of motion to familiarize themselves with the device. A practice trial was also performed to ensure that the subject understood the testing procedure. For each test position, a block was placed at the specific
Fig. 2.
2.2.3. Force sense procedures Force matching was tested with unilateral and contralateral reproduction at 10% and 30% of the MVIC. For the unilateral force sense procedure, the subject was positioned in the same manner as the MVIC test. The subject used the digital readout from the load cell to establish the target force, and once obtained, they were asked to maintain the isometric contraction for 5 sec and then relax. Immediately following, participants were asked to reproduce the target force with the same ankle without the input from the digital readout. A 1-min rest was used between trials and a total of three trials were performed at the initial force. A 5-min rest was then provided prior to repeating the procedures for the second target force. Following another 5-min rest period, the entire process was repeated using the contralateral ankle. The initial ankle side and initial force were randomly assigned between the subjects. Three trials were performed at each force. For the contralateral reproduction, the uninjured ankle produced the reference force and the injured ankle produced the reproduction force. If the subject had no history of ankle injury, one ankle was randomly assigned as the “involved” limb. The purpose of the contralateral reproduction was to detect a bias error between the
Electric goniometer.
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opposite ankles. This was not possible with the unilateral procedures. We suspected that one possible result of an ankle sprain might be a consistent, albeit incorrect, over or under perception of the target force by the injured ankle. The subsequent result would be a difference in stiffness between injured and uninjured ankles. However, the contralateral model may also require a greater level of motor control, thus, revealing differences in control, proprioception, or both. All force sense data were acquired, stored, and analyzed using a PC compatible computer (386 processor, AD-16-330, North Sioux City, SD) and Data Pac 2000 Version 2.40 Lab Applications Systems software (Run Technologies, Laguna Hills, CA).
done in this condition. The process was repeated with two inertial conditions where the external intertia (0.065 and 0.131 kg/cm2) was increased through the addition of weights to the sides of the cradle. We used a leastmeans-square fit of a second order model to the empirical data. The modeled data and the measured data yielded an R squared of 0.98. Zinder [29] has previously reported high reliability and validity of this procedure. Interclass correlation coefficients for day-to-day and trial reliability ranged from 0.93 to 0.96, respectively [29]. The frequency and decay of the rotational oscillations were calculated. From this information, stiffness was calculated in Newton meters per radian (Nm/rad). 2.3. Statistical analysis
2.2.4. Stiffness For the stiffness measurement, each subject stood on a custom-made inversion–eversion cradle device (Zinder, University of Virginia). The cradle was placed on a force platform (Bertec 6700, Columbus OH) to standardize subject positioning (Fig. 3). Prior to beginning testing, the subject’s weight was measured using the force plate, and a visual analog scale displayed percent body weight. The subject stood in a bipedal stance with one foot in the center of the cradle and the contralateral foot on a box adjacent to the cradle. The subject was then instructed to maintain 50% body weight on the cradle, using a visual scale to ensure equal weight distribution. A small weighted ball was then dropped on the corner of the device to perturb the cradle. The perturbation energy was held constant by dropping the ball from a consistent height for all subjects. Each subject was instructed not to assist or interfere with the inversion and eversion motion caused by the perturbation. The transient motion oscillations were recorded using a single turn potentiometer (Clarostat, Mexico City, Mexico) aligned with the axis of rotation of the cradle. Five trials were
Fig. 3.
Error scores were calculated between the reference point and reproduction point for both joint reposition sense and force sense. Constant error (CE) was calculated by the sum of the (reproduction value⫺reference value)/3 trials. Absolute error (AE) was calculated by the sum of the absolute value of the (reproduction value⫺reference value)/3 trials. Absolute constant error (ACE) was calculated from the absolute value of the constant error. All data were imported into SPSS and Pearson product moment correlations were done to determine the relationship between ankle stiffness, force sense and joint reposition sense. A Bonferronni correction was made due to the high number of correlations (0.05 / 18 = 0.003). 3. Results Means and standard deviations for joint reposition sense, force sense, and stiffness are shown in Table 1. We found no significant correlations between force sense
Inversion–eversion cradle.
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Table 1 Means and standard deviation (degrees) Mean
S.D.
Inversion joint reposition sense Constant error Absolute error Absolute constant error
1.53 3.01 2.64
±2.97 ±1.89 ±2.02
Eversion joint reposition sense Constant error Absolute error Absolute constant error
1.64 2.10 1.81
±1.52 ±1.50 ±1.31
Unilateral reproduction force sense 10% MVIC Constant error Absolute error Absolute constant error
0.50 0.91 0.71
±0.85 ±0.63 ±0.67
Unilateral reproduction force sense 30% MVIC Constant error Absolute error Absolute constant error
0.31 1.55 1.14
±1.47 ±0.87 ±0.97
Contralateral reproduction force sense 10% MVIC Constant error Absolute error Absolute constant error
0.59 1.85 1.31
±1.92 ±1.36 ±1.51
0.70 3.31 2.87
±3.86 ±2.48 ±2.66
25.08
±9.32
Contralateral reproduction force sense 30% MVIC Absolute error Absolute constant error Stiffness
and joint reposition sense, with values of r ranging from 0.01 to 0.29, or stiffness and joint reposition sense, with values of r ranging from 0.01 to 0.18. Significant correlations were found between stiffness and force sense. Specifically, contralateral reproduction was significantly correlated to stiffness in the involved ankle (values of r ranging from 0.47 to 0.65; Pⱕ0.003). Correlations for all measures are shown in Tables 2 and 3.
Table 2 Stiffness and joint reposition sense and unilateral force sense correlations Stiffness Inversion joint reposition sense Constant error Absolute error Absolute constant error
⫺0.16 ⫺0.17 ⫺0.18
Eversion joint reposition sense Constant error Absolute error Absolute constant error
0.01 ⫺0.07 ⫺0.01
4. Discussion The sensorimotor system acts to regulate both proprioception and muscle stiffness. It has been hypothesized that partial de-afferentiation, or damage to the mechanoreceptor and associated nerve fiber, occurs following injury to the ankle joint [10]. Thus, both stiffness and proprioception may be altered following injury. The primary finding of this study was that stiffness and force sense were significantly correlated, i.e. increases in force errors were associated with increases in stiffness. Since each correlation was partially computed from error scores, further discussion is necessary on the error calculations used in this study. Constant error calculates
Unilateral reproduction force sense 10% MVIC Constant error Absolute error Absolute constant error
0.09 0.17 0.15
Unilateral reproduction force sense 30% MVIC Constant error Absolute error Absolute constant error
0.11 0.21 0.16
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Table 3 Stiffness and bilateral force sense correlations Involved limb Contralateral reproduction 10% MVIC Constant error Absolute error Absolute constant error
0.51∗ 0.65∗ 0.53∗
Contralateral reproduction 30% MVIC Constant error Absolute error Absolute constant error
0.35 0.47∗ 0.48∗
∗
Significant P ⬍ 0.003.
the average magnitude and direction of the error and is often referred to as bias. Absolute error is the absolute deviation between the reference and reproduction point, and combines the accuracy and variability of the movement. Lastly, absolute constant error is merely the absolute value of the constant error. It is often reported to counteract positive and negative scores that may “cancel” each other out [2]. These error calculations are consistent with what has previously been used in the literature. Therefore, the only error score that accounts for direction is constant error. In the present study, the constant error correlations were positive between the stiffness and contralateral force sense reproduction (10% MVIC r = 0.51, P ⬍ 0.001; 30% MVIC r = 0.35, P = 0.026). The reason for the positive correlation is due to the positive direction of the force sense error. Sixty percent of the subjects overshot the target, resulting in a positive constant error value. The greatest magnitude of error was also in the positive direction, ranging from 0.6 to 6.91 N for target overshoots. Conversely, when undershooting the target, the error only ranged from ⫺0.19 to ⫺2.81 N. Thus, larger overshoots were associated with greater stiffness (Fig. 4). Theoretically, this provides a rationale for the correlation between force sense and stiffness. Subjects that overshoot a target force are incorrectly sensing the amount of tension in the muscles that cross the joint. One potential result of this incorrect afferent information is to recruit more motor units than necessary, producing a greater force response. Similar compensation could occur when regulating stiffness. Thus, during normal activity, the inability to appropriately sense necessary tension could cause greater motor unit recruitment, which in turn causes increased muscle stiffness. Further explanation needs to be provided for why the significant correlation was only seen in the contralateral reproduction. With the unilateral reproduction, the reference and reproduction are done with the same limb, the problem arises that in an injured limb, the afferent information that is processing the reference value may be incorrect and therefore, the participant is simply trying
Fig. 4. Significant relationship between contralateral reproduction 10% MVIC force sense and ankle stiffness.
to reproduce varied and possibly incorrect information. In the contralateral reproduction, the uninjured limb is producing the reference value and therefore ensuring that accurate information be produced. Any deviation in the reproduction of this value could therefore be due to damage to the sensorimotor pathways of the injured limb. A limitation of this study was that the contralateral reproduction was also not used in the joint reposition sense measure. While this was done to mimic what has previously been done in the literature, future research is needed to determine if a similar relationship may exist with contralateral reproduction of joint reposition sense. The question remains if these mechanisms have a cause–effect relationship, or if they both change concurrently due to injury to the somatosensory system. Following Freeman’s hypothesis [10], injury causes deafferentiation and potential alteration in proprioceptive senses. While Freeman’s theory has received much attention, this idea of de-afferentiation following injury has never been confirmed. We are still unable to determine if these deficits in proprioceptive capabilities are due to damage to the peripheral mechanoreceptors themselves or the sensory pathways that carry the afferent information [30]. By evaluating two different measures of proprioception, we also had the opportunity to assess how different receptors may play a role in this relationship. Research has shown that muscle spindles provide information on change in length and rate of change in length, and GTOs provide information on muscle tension [1]. Therefore, it seems suitable to associate muscle spindles with joint reposition sense and GTOs with force sense. Since a significant correlation was found between force sense and stiffness, our data suggest that the mechanism to control stiffness may be more related to GTO function than muscle spindle function. However, joint reposition sense testing may not assess all aspects of the
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muscle spindle causing potential effects on stiffness regulation to go unnoticed. A limitation of this study was the large number of subjects located within one standard deviation of the mean on the proprioceptive and stiffness measures. Since this was a within subjects design, we thought a heterogeneous sample of 40 people would give us adequate information on both proprioception and stiffness measures. We felt adequate sampling in the extremes of these measures were important to assess this relationship. While we were successful in sampling people in these regions with stiffness values ranging from 11.12 to 59.09 Nm/rad (S.D. = 9.3 Nm / rad), joint reposition sense errors ranging from 0 to 8.8 deg (S.D. = 1.8 deg), and force sense errors ranging 0 to 13.41 N (S.D. = 1.5 N), the actual number of subjects in the extremes was very low. Three subjects had considerably higher than average stiffness values, ranging from 47.64 to 59.09 Nm/rad. In two of the three cases, the high values were consistent for the right and left sides. These two subjects also had considerably higher contralateral reproduction force sense errors, overshooting the target by 5.97–13.41 N. This provides some confirmation that these two factors are in fact related, but due to the low number of subjects in this high range of stiffness we feel additional testing is necessary.
5. Conclusion This was an exploratory investigation that evaluated the relationship between joint reposition sense and force sense with ankle stiffness. Our results show that force sense and ankle stiffness are correlated. Whether the decreased ability to appropriately sense force (increased error) sends information to the central nervous system to increase muscle stiffness in response to an unexpected loss of stability, or whether these two phenomena function independently and both change concurrently as a result of injury to the system is up for debate. We do not find it appropriate to conclude that there is no relationship between joint reposition sense and stiffness; simply we did not find it in this investigation. Continued research is necessary to further elucidate these relationships.
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Relationship between two proprioceptive measures and stiffness at the ankle Carrie L. Docherty a,∗, Brent L. Arnold b, Steven M. Zinder a, Kevin Granata c, Bruce M. Gansneder a a
Curry School of Education, University of Virginia, 210 Emmet St South, Suite #203, P.O. Box 400407, Charlottesville, VA 22904-4407, USA b School of Education, Virginia Commonwealth University, Richmond, VA, USA c School of Medicine, University of Virginia, Charlottesville, VA, USA Received 8 October 2002; received in revised form 25 February 2003; accepted 27 February 2003
Abstract Previous research has investigated the role of proprioception and stiffness in the control of joint stability. However, to date, no research has been done on the relationship between proprioception and stiffness. Therefore, the purpose of this study was to determine the relationship between force sense, joint reposition sense, and stiffness at the ankle. A heterogeneous sample was obtained for this study; 20 of the 40 participants had a history of ankle sprains, and 13 of the 20 had been diagnosed by a physician (two mild ankle sprains, seven moderate sprains, four severe sprains). All subjects were asymptomatic and active at the time of the study. Active joint reposition sense was measured using a custom-built ankle goniometer, force sense was measured unilaterally and contralaterally with a load cell, and ankle muscle stiffness was measured via transient oscillation using a custom-built inversion– eversion cradle. We found no significant correlations between stiffness and joint reposition sense, with values of r ranging from 0.01 to 0.21. Significant correlations were found between stiffness and force sense. Specifically, contralateral force sense reproduction was significantly correlated to stiffness in the injured or “involved” ankle (r’s ranging from 0.47 to 0.65; Pⱕ0.008). Whether the decreased ability to appropriately sense force (increased error) sends information to the central nervous system to increase muscle stiffness in response to an unexpected loss of stability, or whether these two phenomena function independently and both change concurrently as a result of injury to the system requires further investigation. 2003 Elsevier Ltd. All rights reserved. Keywords: Joint reposition sense; Force sense; Force matching; Joint stability
1. Introduction Loss of stability has been theorized to be a primary cause of joint injury. Joint stability is the ability to maintain or quickly return to proper positioning following a perturbation [1]. Maintenance of joint stability is mediated by the sensorimotor system through a combination of feedforward and feedback controls. The feedforward process prepares the system for the upcoming motor command and receipt of feedback information [2]. Feedback is a continual process of gaining information via the afferent pathways and is primarily regulated from
Corresponding author. Tel.: +1-434-242-7490; fax: +1-434-9241389. E-mail address: [email protected] (C.L. Docherty). ∗
1050-6411/$ - see front matter 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S1050-6411(03)00035-X
previous experiences. Both proprioception and muscle stiffness utilize these controls to facilitate proper movement patterns, and more importantly, protect against injury. Proprioception and stiffness both contribute to joint stability, but little research has been conducted to determine if there is a relationship between the two factors. In proprioception, input is received from the peripheral afferents (muscle spindles, joint receptors, cutaneous receptors, and golgi tendon organs (GTOs)) [3], and provides information on limb awareness, position, force, and heaviness. Conscious proprioception senses include kinesthesia, joint position sense, and sense of force [1,4]. Considerable research has been done to explain how injuries affect these proprioceptive capabilities [5–9]. In 1965, Freeman [10] hypothesized that partial de-afferentiation occurs following an ankle injury and leads to
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proprioceptive deficits. This deficit has been confirmed by multiple studies that link functional instability to deficits in proprioceptive capabilities of the ankle [5–9]. While kinesthesia and joint reposition sense have been continually used to assess proprioceptive function at the ankle, force sense has received little attention. Force sense, or sense of heaviness, was one of the earliest methods used to assess peripheral and central control of joint movement dating back to 1834, but modern researchers have failed to further develop this theory at the ankle. Force sensation is defined as the ability to perceive a given force during a voluntary contraction. Testing can be done with unilateral reproduction, contralateral reproduction, or simultaneous reproduction [11]. To date, the majority of force sense research has been done in the upper extremity [12,13]. Only recently has force sense been examined at the ankle, with the purpose of re-establishing this procedure. Using unilateral reproduction, trial reliability was assessed at 50% and 75% maximal voluntary isometric contraction (MVIC). All testing was done in normal, uninjured subjects. Trial reliability was found to be high, with r’s ranging from 0.82–0.89 [14]. The central nervous system receives proprioceptive feedback from the joint via afferent pathways, the same paths used to determine appropriate levels of muscle stiffness [15–18]. Muscle stiffness is the combination of active and passive stiffness, defined as the ratio of change in force to change in length [15]. Active muscle stiffness can be further broken down into intrinsic and reflex stiffness [19]. Intrinsic muscle stiffness provides the first line of defense following a perturbation and is contingent on the level of muscle activation, or the number of actin and myosin bonds, at the time of the perturbation [20–22]. Reflexes have also been shown to increase muscle stiffness, but due to timing issues, the reflexes do not occur quickly enough to protect certain joints against injury [16,17]. However, the reflexes do play an important role in preprogramming the stiffness via the afferent information from previous perturbations [15]. Research has shown that stiffness can protect the joint through limiting excessive joint translations and subsequent ligament strain caused by an external perturbation [23–26]. Muscle spindle afferents play a large role in regulating both muscle stiffness and position and movement sense [27], yet the relationship between proprioception and muscle stiffness is poorly understood. We hypothesized that inappropriate function of the afferent pathways would adversely affect accurate awareness of length and/or tension in the musculotendinous structure and muscle stiffness. Therefore, the purpose of this paper was to evaluate the relationship between force sense, joint reposition sense and stiffness at the ankle joint.
2. Methods 2.1. Subjects Forty healthy college students (11 males, 29 females, 23.2 ± 5.0 years; 168.4 ± 8.6 cm; 68.5 ± 12.1 kg) from a large university volunteered for this study. Each subject completed an orthopedic questionnaire prior to beginning the study. The information obtained from this questionnaire assisted in assuring that a heterogeneous sample was obtained for this study; 20 had a history of ankle sprains to one ankle, 13 of the 20 had been diagnosed by a physician (two mild ankle sprains, seven moderate sprains, four severe sprains), and 18 of the 20 had a history of giving way episodes. All subjects were asymptomatic and active at the time of the study. The University’s Human Investigation Committee approved the study, and all subjects read and signed a written informed consent form prior to beginning testing. 2.2. Test procedures Each subject came to the sports medicine research laboratory on three occasions. During the initial session, the subjects completed the orthopedic questionnaire, MVIC testing, and active joint reposition sense testing. On the second occasion, the subjects performed the force matching protocol, and on the third day, ankle stiffness was measured. All testing was done bilaterally for each of the test conditions. 2.2.1. Maximal voluntary isometric contraction All subjects were barefoot during the testing procedures, and peak force was measured to the nearest 0.1 N. Maximal eversion strength was tested in both ankles. For this procedure, a load cell (Sensotec, Columbus, OH) with a digital readout was mounted to the wall. The subject was positioned supine on a treatment table with the knees flexed to approximately 10°. The thighs were also fixed to minimize involvement of the quadriceps, hamstrings, and gluteus muscles. The foot was placed off the end of the table and attached to the load cell with Velcro straps (Fig. 1). The subject was instructed to maximally evert the foot for 5 sec. This was repeated for three trials, with a 10-sec rest between trials. The average of the three peak isometric values were recorded as the subject’s MVIC. 2.2.2. Joint reposition sense testing Joint reposition sense measurements were taken with a custom-designed electric goniometer [28]. The device was blocked so only inversion and eversion motion could be performed. All subjects were barefoot during the testing and the foot was placed in a heel cup that was directly mounted to the footplate. The lower leg was supported in the leg rest in full extension and both the
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point in the range of motion. The subject was instructed to actively move the foot until the footplate hit the block. Once in the test position, subjects were told to concentrate on the position for 15 sec. The block was then removed, and the subjects were instructed to move the foot to the opposite extreme of motion and then back to the test position. The reference and reproduction angle measurement were recorded from the electronic readout to the nearest tenth of a degree (0.1°). This procedure was repeated for three trials at each test angle with each ankle.
Fig. 1.
Subject positioning for MVIC and force sense procedures.
leg and foot were fastened in position (Fig. 2). The footplate was positioned to place the ankle in subtalar joint neutral (STJN), and the goniometer was set at zero. The subjects closed their eyes throughout the remainder of testing to eliminate any visual cues. All subjects were tested at 20° from STJN for inversion and at 10° from STJN for eversion. Initially, the subjects were asked to move the foot into the extremes of the range of motion to familiarize themselves with the device. A practice trial was also performed to ensure that the subject understood the testing procedure. For each test position, a block was placed at the specific
Fig. 2.
2.2.3. Force sense procedures Force matching was tested with unilateral and contralateral reproduction at 10% and 30% of the MVIC. For the unilateral force sense procedure, the subject was positioned in the same manner as the MVIC test. The subject used the digital readout from the load cell to establish the target force, and once obtained, they were asked to maintain the isometric contraction for 5 sec and then relax. Immediately following, participants were asked to reproduce the target force with the same ankle without the input from the digital readout. A 1-min rest was used between trials and a total of three trials were performed at the initial force. A 5-min rest was then provided prior to repeating the procedures for the second target force. Following another 5-min rest period, the entire process was repeated using the contralateral ankle. The initial ankle side and initial force were randomly assigned between the subjects. Three trials were performed at each force. For the contralateral reproduction, the uninjured ankle produced the reference force and the injured ankle produced the reproduction force. If the subject had no history of ankle injury, one ankle was randomly assigned as the “involved” limb. The purpose of the contralateral reproduction was to detect a bias error between the
Electric goniometer.
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opposite ankles. This was not possible with the unilateral procedures. We suspected that one possible result of an ankle sprain might be a consistent, albeit incorrect, over or under perception of the target force by the injured ankle. The subsequent result would be a difference in stiffness between injured and uninjured ankles. However, the contralateral model may also require a greater level of motor control, thus, revealing differences in control, proprioception, or both. All force sense data were acquired, stored, and analyzed using a PC compatible computer (386 processor, AD-16-330, North Sioux City, SD) and Data Pac 2000 Version 2.40 Lab Applications Systems software (Run Technologies, Laguna Hills, CA).
done in this condition. The process was repeated with two inertial conditions where the external intertia (0.065 and 0.131 kg/cm2) was increased through the addition of weights to the sides of the cradle. We used a leastmeans-square fit of a second order model to the empirical data. The modeled data and the measured data yielded an R squared of 0.98. Zinder [29] has previously reported high reliability and validity of this procedure. Interclass correlation coefficients for day-to-day and trial reliability ranged from 0.93 to 0.96, respectively [29]. The frequency and decay of the rotational oscillations were calculated. From this information, stiffness was calculated in Newton meters per radian (Nm/rad). 2.3. Statistical analysis
2.2.4. Stiffness For the stiffness measurement, each subject stood on a custom-made inversion–eversion cradle device (Zinder, University of Virginia). The cradle was placed on a force platform (Bertec 6700, Columbus OH) to standardize subject positioning (Fig. 3). Prior to beginning testing, the subject’s weight was measured using the force plate, and a visual analog scale displayed percent body weight. The subject stood in a bipedal stance with one foot in the center of the cradle and the contralateral foot on a box adjacent to the cradle. The subject was then instructed to maintain 50% body weight on the cradle, using a visual scale to ensure equal weight distribution. A small weighted ball was then dropped on the corner of the device to perturb the cradle. The perturbation energy was held constant by dropping the ball from a consistent height for all subjects. Each subject was instructed not to assist or interfere with the inversion and eversion motion caused by the perturbation. The transient motion oscillations were recorded using a single turn potentiometer (Clarostat, Mexico City, Mexico) aligned with the axis of rotation of the cradle. Five trials were
Fig. 3.
Error scores were calculated between the reference point and reproduction point for both joint reposition sense and force sense. Constant error (CE) was calculated by the sum of the (reproduction value⫺reference value)/3 trials. Absolute error (AE) was calculated by the sum of the absolute value of the (reproduction value⫺reference value)/3 trials. Absolute constant error (ACE) was calculated from the absolute value of the constant error. All data were imported into SPSS and Pearson product moment correlations were done to determine the relationship between ankle stiffness, force sense and joint reposition sense. A Bonferronni correction was made due to the high number of correlations (0.05 / 18 = 0.003). 3. Results Means and standard deviations for joint reposition sense, force sense, and stiffness are shown in Table 1. We found no significant correlations between force sense
Inversion–eversion cradle.
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Table 1 Means and standard deviation (degrees) Mean
S.D.
Inversion joint reposition sense Constant error Absolute error Absolute constant error
1.53 3.01 2.64
±2.97 ±1.89 ±2.02
Eversion joint reposition sense Constant error Absolute error Absolute constant error
1.64 2.10 1.81
±1.52 ±1.50 ±1.31
Unilateral reproduction force sense 10% MVIC Constant error Absolute error Absolute constant error
0.50 0.91 0.71
±0.85 ±0.63 ±0.67
Unilateral reproduction force sense 30% MVIC Constant error Absolute error Absolute constant error
0.31 1.55 1.14
±1.47 ±0.87 ±0.97
Contralateral reproduction force sense 10% MVIC Constant error Absolute error Absolute constant error
0.59 1.85 1.31
±1.92 ±1.36 ±1.51
0.70 3.31 2.87
±3.86 ±2.48 ±2.66
25.08
±9.32
Contralateral reproduction force sense 30% MVIC Absolute error Absolute constant error Stiffness
and joint reposition sense, with values of r ranging from 0.01 to 0.29, or stiffness and joint reposition sense, with values of r ranging from 0.01 to 0.18. Significant correlations were found between stiffness and force sense. Specifically, contralateral reproduction was significantly correlated to stiffness in the involved ankle (values of r ranging from 0.47 to 0.65; Pⱕ0.003). Correlations for all measures are shown in Tables 2 and 3.
Table 2 Stiffness and joint reposition sense and unilateral force sense correlations Stiffness Inversion joint reposition sense Constant error Absolute error Absolute constant error
⫺0.16 ⫺0.17 ⫺0.18
Eversion joint reposition sense Constant error Absolute error Absolute constant error
0.01 ⫺0.07 ⫺0.01
4. Discussion The sensorimotor system acts to regulate both proprioception and muscle stiffness. It has been hypothesized that partial de-afferentiation, or damage to the mechanoreceptor and associated nerve fiber, occurs following injury to the ankle joint [10]. Thus, both stiffness and proprioception may be altered following injury. The primary finding of this study was that stiffness and force sense were significantly correlated, i.e. increases in force errors were associated with increases in stiffness. Since each correlation was partially computed from error scores, further discussion is necessary on the error calculations used in this study. Constant error calculates
Unilateral reproduction force sense 10% MVIC Constant error Absolute error Absolute constant error
0.09 0.17 0.15
Unilateral reproduction force sense 30% MVIC Constant error Absolute error Absolute constant error
0.11 0.21 0.16
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Table 3 Stiffness and bilateral force sense correlations Involved limb Contralateral reproduction 10% MVIC Constant error Absolute error Absolute constant error
0.51∗ 0.65∗ 0.53∗
Contralateral reproduction 30% MVIC Constant error Absolute error Absolute constant error
0.35 0.47∗ 0.48∗
∗
Significant P ⬍ 0.003.
the average magnitude and direction of the error and is often referred to as bias. Absolute error is the absolute deviation between the reference and reproduction point, and combines the accuracy and variability of the movement. Lastly, absolute constant error is merely the absolute value of the constant error. It is often reported to counteract positive and negative scores that may “cancel” each other out [2]. These error calculations are consistent with what has previously been used in the literature. Therefore, the only error score that accounts for direction is constant error. In the present study, the constant error correlations were positive between the stiffness and contralateral force sense reproduction (10% MVIC r = 0.51, P ⬍ 0.001; 30% MVIC r = 0.35, P = 0.026). The reason for the positive correlation is due to the positive direction of the force sense error. Sixty percent of the subjects overshot the target, resulting in a positive constant error value. The greatest magnitude of error was also in the positive direction, ranging from 0.6 to 6.91 N for target overshoots. Conversely, when undershooting the target, the error only ranged from ⫺0.19 to ⫺2.81 N. Thus, larger overshoots were associated with greater stiffness (Fig. 4). Theoretically, this provides a rationale for the correlation between force sense and stiffness. Subjects that overshoot a target force are incorrectly sensing the amount of tension in the muscles that cross the joint. One potential result of this incorrect afferent information is to recruit more motor units than necessary, producing a greater force response. Similar compensation could occur when regulating stiffness. Thus, during normal activity, the inability to appropriately sense necessary tension could cause greater motor unit recruitment, which in turn causes increased muscle stiffness. Further explanation needs to be provided for why the significant correlation was only seen in the contralateral reproduction. With the unilateral reproduction, the reference and reproduction are done with the same limb, the problem arises that in an injured limb, the afferent information that is processing the reference value may be incorrect and therefore, the participant is simply trying
Fig. 4. Significant relationship between contralateral reproduction 10% MVIC force sense and ankle stiffness.
to reproduce varied and possibly incorrect information. In the contralateral reproduction, the uninjured limb is producing the reference value and therefore ensuring that accurate information be produced. Any deviation in the reproduction of this value could therefore be due to damage to the sensorimotor pathways of the injured limb. A limitation of this study was that the contralateral reproduction was also not used in the joint reposition sense measure. While this was done to mimic what has previously been done in the literature, future research is needed to determine if a similar relationship may exist with contralateral reproduction of joint reposition sense. The question remains if these mechanisms have a cause–effect relationship, or if they both change concurrently due to injury to the somatosensory system. Following Freeman’s hypothesis [10], injury causes deafferentiation and potential alteration in proprioceptive senses. While Freeman’s theory has received much attention, this idea of de-afferentiation following injury has never been confirmed. We are still unable to determine if these deficits in proprioceptive capabilities are due to damage to the peripheral mechanoreceptors themselves or the sensory pathways that carry the afferent information [30]. By evaluating two different measures of proprioception, we also had the opportunity to assess how different receptors may play a role in this relationship. Research has shown that muscle spindles provide information on change in length and rate of change in length, and GTOs provide information on muscle tension [1]. Therefore, it seems suitable to associate muscle spindles with joint reposition sense and GTOs with force sense. Since a significant correlation was found between force sense and stiffness, our data suggest that the mechanism to control stiffness may be more related to GTO function than muscle spindle function. However, joint reposition sense testing may not assess all aspects of the
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muscle spindle causing potential effects on stiffness regulation to go unnoticed. A limitation of this study was the large number of subjects located within one standard deviation of the mean on the proprioceptive and stiffness measures. Since this was a within subjects design, we thought a heterogeneous sample of 40 people would give us adequate information on both proprioception and stiffness measures. We felt adequate sampling in the extremes of these measures were important to assess this relationship. While we were successful in sampling people in these regions with stiffness values ranging from 11.12 to 59.09 Nm/rad (S.D. = 9.3 Nm / rad), joint reposition sense errors ranging from 0 to 8.8 deg (S.D. = 1.8 deg), and force sense errors ranging 0 to 13.41 N (S.D. = 1.5 N), the actual number of subjects in the extremes was very low. Three subjects had considerably higher than average stiffness values, ranging from 47.64 to 59.09 Nm/rad. In two of the three cases, the high values were consistent for the right and left sides. These two subjects also had considerably higher contralateral reproduction force sense errors, overshooting the target by 5.97–13.41 N. This provides some confirmation that these two factors are in fact related, but due to the low number of subjects in this high range of stiffness we feel additional testing is necessary.
5. Conclusion This was an exploratory investigation that evaluated the relationship between joint reposition sense and force sense with ankle stiffness. Our results show that force sense and ankle stiffness are correlated. Whether the decreased ability to appropriately sense force (increased error) sends information to the central nervous system to increase muscle stiffness in response to an unexpected loss of stability, or whether these two phenomena function independently and both change concurrently as a result of injury to the system is up for debate. We do not find it appropriate to conclude that there is no relationship between joint reposition sense and stiffness; simply we did not find it in this investigation. Continued research is necessary to further elucidate these relationships.
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