Quantifying the Deep Tendon Reflex Using Varying ... - IEEE Xplore

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Quantifying the Deep Tendon Reflex Using Varying Tendon Indentation Depths: Applications to Spasticity Matthieu K. Chardon, W. Zev Rymer, and Nina L. Suresh

Abstract—The deep tendon reflex (DTR) is often utilized to characterize the neuromuscular health of individuals because it is cheap, quick to implement, and requires limited equipment. However, DTR assessment is unreliable and assessor-dependent improve the reliability of the DTR assessment, we devised a novel standardization procedure. Our approach is based on the hypothesis that the neuromuscular state of a muscle changes systematically with respect to the indentation depth of its tendon. We tested the hypothesis by progressively indenting the biceps tendons on each side of nine hemiplegic stroke survivors to different depths, and then superimposing a series of brief controlled taps at each indentation depth to elicit a reflex response. Our results show that there exists a unique indentation depth at which reflex responses are consistently recorded (termed the Reflex Threshold) with increasing amplitude along increasing indentation depth. We further show that the reflex threshold depth is systematically smaller on the affected side of stroke survivors and that it is negatively correlated with the Modified Ashworth Score (VAF 70%). Our procedure also enables measurement of passive mechanical properties at the indentation location. In conclusion, our study shows that controlling for the indentation depth of the tendon of a muscle alters its reflex response predictably. Our novel device and method could be used to estimate neuromuscular changes in muscle (e.g., spasticity). Although some refinement is needed, this method opens the door to more reliable quantification of the DTR. Index Terms—Deep tendon reflex, reflex threshold, skeletal muscle mechanical properties, spasticity, stroke.

I. INTRODUCTION

O

NE of the comorbidities of stroke is spasticity, in which paretic muscles show heightened reflex responses to stretch. It is estimated that more than one third of people recovering from a stroke develop this painful and debilitating condition [1]–[4]. Yet, despite its prevalence, there remains no adequate method of quantifying its presence and magnitude in spastic patients. Lance 1980 provided a widely used definition of spasticity as: “a motor disorder characterized by exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex, as one component of the upper motor neuron syndrome” [5]. Many Manuscript received November 28, 2012; revised August 02, 2013, November 19, 2013; accepted December 12, 2013. Date of publication January 13, 2014; date of current version March 05, 2014. M. K. Chardon is with the Department of Biomedical Engineering, Northwestern University, Evanston, IL 60208 USA. W. Z. Rymer is with the Department of Research, Rehab Institute of Chicago, Chicago, IL 60611 USA. N. L. Suresh is with the Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, IL 60611 USA Digital Object Identifier 10.1109/TNSRE.2014.2299753

investigators have thus sought to quantify the stretch reflex response as a means to estimate the severity of spasticity [6]–[13]. Several published approaches are based on assessing the deep tendon reflex (DTR or tendon jerk), where a tendon hammer is used to strike the tendon of a muscle in order to evaluate the occurrence, strength, and duration of the reflex response. Using either the Mayo Clinic scale for tendon reflex assessment or the National Institute of Neurological Disorders and Stroke (NINDS) myotatic reflex scale, a number is assigned to the intensity of the response [14], [15]. Even though these scales have shown inconclusive intra- and inter-observer reliability ([11], [16], [17]) the tendon hammer is widely used in the clinic to assess spasticity because the test is quick to perform, requires minimal training, and involves virtually no equipment cost. To improve the reliability of the DTR test in the clinic, researchers, engineers and designers have sought to control the stimulus delivered by the tendon hammer onto the tendon as well as to standardize the DTR’s response. To control the stimulus one needs to control the energy delivered onto the tendon thus techniques ranging from a standardized tendon hammer drop, to a preloaded spring gun, to a computer controlled ballistic tap have all been tried. The response of the DTR has been standardized with measures including electromyography (EMG), force and acceleration [12], [14], [18]–[37]. Over the years, with controlled input and accurate measures, research showed that the DTR is dependent on tap intensity, muscle background activity and limb placement. Research also showed that DTR measurements poorly correlated with other common measures of spasticity such as the Modified Ashworth Score (MAS) [7], [9]. In short, even with ongoing attempts towards standardization, DTR measurements require further refinement for accurate quantification. We believe that these limitations are due, in part, to the way the DTR has been tested thus far. Three basic physiological principles of the stretch reflex and of muscle properties have been largely ignored. First the stretch reflex response is critically dependent on the stimulus parameters such as the length change and the velocity of the muscle. Traditionally, the tendon hammer stretches the muscle by tapping the tendon in a ballistic manner, where it is not possible to control for the length and the velocity of the muscle. Second, the impact location of the hammer on the tendon is often variable, resulting in a variable muscle length change and thus variable reflex response magnitude [38]. Third, the initial length of the muscle is often not well controlled by the examiner, even though it also affects the intensity of the reflex response [39], [40]. In an earlier study from our research group we dealt with the first two limitations of the DTR test. We utilized a position

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TABLE I

controlled actuator to deliver tendon taps with fixed positionand velocity profiles, while recording the tap of the force with a load cell placed adjacent to the tapper head [34]. During reflex testing, the tapper head was also placed in contact with the skin over the tendon using a mechanical holder, in order to reduce the variability of tap location that can occur during taps. The indentation position of the tapper head, which indirectly controls the passive muscle length, was only qualitatively controlled. The main objective of this study was therefore to systematically change the length of the muscle prior to each tap, to explore the dependence of the traditional DTR on the initial length of muscle (the third limitation of the standard DTR testing protocols). We developed a device and protocol such that after contact with the skin over the tendon, the tapper would be progressively lowered onto the tendon, progressively indenting the skin–adipose–tendon–muscle (SATM) complex in the process, allowing for the exploration of the SATM complex at different initial conditions. We hypothesize that the neuromuscular state of a muscle changes systematically as we change the preload on its tendon. To explore the effects of changing the initial conditions we superimpose brief controlled taps at each depth to elicit a reflex response. We will describe the experimental device and the experimental protocol designed for this experiment. An introduction to this work was presented in prior conference proceedings [41], [42]. II. METHOD A. Participants Nine hemiplegic spastic stroke survivors were recruited to test our approach. Participants had sustained a single hemispheric stroke at least six months prior to experimental testing. Spasticity was measured by a physical therapist using the Modified Ashworth Score assessment. Subjects had to exhibit a score to be included in the study (Table I). After completing the procedure on the affected side, patients were asked to return to be tested on their contralateral limbs. All participants gave informed consent via protocols approved by the Institutional Review Board under the Office for the Protection of Human Subjects at Northwestern University. B. Experimental Setup 1) Experimental Device: The experimental device is composed of a high-resolution (5 m) position-controlled linear ac-

Fig. 1. Schematics of experimental device. (A) Side view of the device with its general dimensions. The device is comprised of three major parts: the force sensor, the linear actuator and the mechanical support (micrometer and magnetic base). (B) Different degrees of freedom (DOF) that the mechanical support provides. (C) Devices in the experimental setting. The device is adjusted such that the tip of the device is placed on the distal tendon of the biceps of brachii.

tuator (Linmot S.A., Spreitenbach, Switzerland) mounted onto a custom frame with three rotational (R1, R2, R3) and three linear degrees of freedom (L1, L2, L3) [Fig. 1(A) and (B)]. The last degree of freedom (L3) is controlled by a manual micrometer (Velmex, Bloomfield, NY, USA), providing sub millimeter (1/10 mm) accuracy of the end effector. The custom frame allows for the placement of tip of the linear actuator anywhere in space in a repeatable and controlled fashion. Internal to the Linmot motor controller lays a PID controller for position error correction, as well as a feedforward model of the device. We tuned the controller to achieve a rise time of 3 ms, an overshoot of 8% and a settling time of 10 ms. When load-free, the controller produces a repeatable tap of an accuracy of mm. This performance does not deteriorate until we reach high loads (14 N) where we observe a loss of approximately 20% in tap height to 0.81 mm ( mm) and a loss in velocity of 18%. The maximum acceleration remains constant for the loads tested. At the tip of the linear actuator we attached a single axis compression/tension load cell (Sensotec miniature mid-range load cell Model 31, Honeywell, Columbus, OH, USA). This sensor can measure up to 50 N (accuracy %) of force both in compression and tension. Throughout this experimental procedure, the load cell measured the compression force of the SATM complex at the distal tendon at the biceps brachii of either the affected or contralateral side of the subjects [Fig. 1(C)]. This experimental device was able to: 1) deliver a repeatable and controlled stimulus; 2) allow the observer to place and hold the tip

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Fig. 2. Schematic of indentation sequence delivered by the tip of the experimental device onto the distal biceps of the subject. The actuator of the experimental device is position-controlled such that it follows the demand sequence. (A) Initial three segments of the sequence. The first sequence starts at the skin of the individual where five triangular taps are delivered. The second sequence is the same as the previous except that the initial indentation position has changed to the new depth of 1 mm. This cycle is repeated until the tip of the device reaches 30 mm. (B) A single sequence of taps for a given indentation position. The series of taps is 12.5 s long and each tap is 2.5 s apart. (C) An ideal single tap. The tap was designed to be 4 ms long and 1 mm deep such that the reflex component of the response (15–20 ms) was not altered by the tap.

in space for all positions within the custom frame range of motion; and 3) record the compression force between the tip and the tested area. 2) Experimental Protocol: The subjects were seated and secured to a Biodex chair (Shirley, NY, USA) by Velcro straps across their torso, from shoulder to hip. We then casted the subject’s wrist and lower arm on the side to be tested. Before the cast cured, the subject’s casted lower arm was clamped at the wrist to a custom magnetic base placed on a steel table [Fig. 1(C)]. The limb was adjusted with a manual goniometer such that the shoulder abduction was 45 , the shoulder flexion was 20 , the elbow extension was 120 and the lower arm abduction was 45 . The linear actuator long-axis was oriented at 90 to the biceps’ distal tendon and the depth was zeroed visually at the surface of the skin. The position of the linear actuator was continuously computer-monitored, guaranteeing repeatability in the stimuli and in the measurements of the reflex.

To record the EMG, we placed surface electrodes (Delsys, Boston, MA, USA) on the medial and lateral heads of both the biceps brachii and the triceps brachii. The EMG record from the triceps brachii was used to determine if there was co-contraction activity. The electrodes were placed near the center of the muscle. With the subject position secured and the EMG electrodes and device in place, we began the preloading and tapping protocol with the tip of the linear actuator. Because the linear actuator was position-controlled, we were able to devise a novel tapping procedure with two distinctive phases. Indentation Phase: The indentation phase changed the indentation position of the tip of the tendon tapper on the SATM complex. The tip of the tendon tapper was indented into the SATM complex with a series of slow 1 mm “ramp and hold” position sequences [Fig. 2(A)]. After each ramp a new indentation position was reached, in effect setting a new initial condition at the SATM complex. Transient Tap Phase: At each indentation position (starting at skin), we superimposed five brief taps at an interval of 2.5 s [Fig. 2(B) and (C)]. The preload phase and transient tap phase were repeated over a total indentation distance of 30 mm into the SATM complex, or to a point tolerated by the subject. The subject was asked to relax during the whole trial. To confirm that the subject’s muscle was quiescent, we checked that the EMG was at baseline prior to each tap for all the indentation positions. The full indentation protocol lasted at most 10 min. 3) Data Collection: We recorded the compression force between the SATM complex and the actuator using the load cell at the tip of the linear actuator. The force measured represents the “pushback” force from the SATM complex. Force data were low pass Butterworth filtered (cut-off 600 Hz) and sampled at 1 kHz (Power 1401, CED, Cambridge, U.K.). The EMG signals were recorded using a Delsys Bagnoli system (Boston, MA, USA). The raw EMG was filtered (20–450 Hz) then amplified by a gain of 100. The surface EMG was sampled at 2 kHz (Power 1401, CED, Cambridge, U.K.). The software Spike2 (ver. 6) was used to collect and synchronize all the signals and control the recording sessions. C. Data Analysis To illustrate this protocol, we will describe a typical set of raw traces (Fig. 3). We will then explain how we analyzed the data. 1) Force Measure of the SATM Complex: a) Raw Force Trace: Fig. 3(A)-Left, shows the raw force response of the distal biceps SATM complex to the five taps (red arrows) at an indentation position of 13 mm. For each of the taps, the force trace can be split into three phases: Preload Phase (I), Tap Phase (II), and Response Phase (III) (Fig. 3(A)-Middle). The Preload Phase (I) is defined as the portion of the force trace prior to the tap event. It is flat and represents the resting mechanical state of the SATM complex. The Tap Phase (II) is the portion of the trace in between the tap event and the reflex response. This portion of the trace represents the passive viscoelastic properties of the muscle recorded prior to the reflex

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Fig. 3. Measures from the SATM complex and the EMG from the biceps brachii of a subject. (A and B Left) Raw traces from the force sensor at the tip of the tendon tapper and the EMG of the biceps brachii for an indentation position of 13 mm. At this indentation, the five triangular taps elicited five responses. (A and B Middle) One of the responses from the raw traces for both the force and the EMG. Both signals have three phases (I, II, and III) each representing the time prior to the tap event (I), the time after the tap event but before the reflex response (II) and the time after the tap event that shows a reflex response (III). The SATM , the tap force and the average raw maximum reflex force . The complex values extracted from the raw trace are the average preload force and the rectified integrated EMG of the reflex response . (A and B EMG values extracted are the rectified integrated EMG prior to the tap event Left) Final results of the analysis using the values extracted for all indentation positions. The SATM complex plot is the maximum reflex force adjusted for preload as a function of the indentation position. The EMG plot is the rectified integrated EMG percentage as a function of the indentation position. Both of these plots show an inflection point at the indentation position 10 mm.

response. The Response Phase (III) represents the reflex portion of the response from the tap. b) SATM Complex Force Values: For each of the phases, we extracted the following variables: the preload force from Phase (I); the maximum tap force from Phase (II); and the maximum reflex force from Phase (III) (Fig. 3(A)-Middle). Preload Force: The preload force is calculated by computing the mean value of a 350 ms window of the force trace prior to each of the transient taps (Fig. 3(A)-Middle— is the mean of the blue trace). For each indentation position, we calculated a preload force value for each of the five taps. The preload force represents the passive force of the SATM complex prior to each tap. It can be used to derive a measure of the passive stiffness of the SATM complex. Maximum Tap Force: is the relative value of the force between the absolute tap force value, , and its corre-

sponding preload value , such that . is calculated by finding the maximum force value within a 10 ms window right after each tap on the force trace (Fig. 3A-Middle— is in red). The maximum tap force provides information regarding the viscoelastic properties of the SATM complex. Maximum Reflex Force: We computed the maximum reflex force , which is the relative force value between the absolute reflex force, , and its corresponding preload , such that, . is found by computing the mean of the trace that is within a window of ms centered on the absolute maximum value of the reflex response (Fig. 3(A)-Middle— is the mean of the green trace). Throughout this study, is used as an estimate of the level of activity generated by the muscle after it is perturbed by a tap event. For example, if the muscle is unresponsive to a tap

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event, the value of is close to zero because the response value is very close to the preload. 2) EMG Measure: a) Raw Rectified EMG Trace: Fig. 3(B)-Left, shows the raw rectified EMG response for the sequence of the five tap events (red arrows). Just as shown in the force trace, the EMG trace exhibits: Preload Phase (I), Tap Phase (II), and Response Phase (III), which are shown in Fig. 3(B)-Middle. The Preload Phase (I) represents the EMG trace prior to the tap. It is the baseline EMG before a response and shows if the muscle is active before a tap. The Tap Phase (II) represents the EMG trace between the tap event and the reflex response. This trace should ideally be identical to the Preload Phase, and should last about 20 ms. The Response Phase (III) represents the EMG activity of the reflex response. b) Biceps Brachii EMG Activity: To quantify the activity of the surface EMG, we computed the rectified-integrated EMG (RIEMG) of the response with respect to the baseline. First, the EMG trace was rectified and integrated over a window pre- and post-stimulus (green and blue traces, Fig. 3(B)-Middle). The RIEMG was then calculated with the following relation: (1) where is the rectified voltage post-stimulus and is the rectified voltage pre-stimulus. The same integration window was used for the baseline and for the response. 3) Data Reduction: For each indentation position, we computed five values of and RIEMG corresponding to the response to the five taps. As an example, and RIEMG from the same side of a subject were plotted against indentation position (Fig. 3(A) and (B)-Right). Even though we present the method for extracting , we will not show corresponding results at this point. D. Statistical Analysis 1) Passive Stiffness Calculation: The passive stiffness of the SATM complex is estimated from the slope of the regression line of the preload force/indentation position curve. In all our subjects, there exists an indentation position (inflection point), at which the passive stiffness slope changes. To identify potential inflection points in the passive stiffness curves, we developed a custom algorithm to search for the presence of these inflection points. For each sequence of preload force values we fit a linear curve to the data. If the variance accounted for (VAF) was 95% or greater then no inflection points were reported. If the VAF was below 95% we used the optimization routine fmincon (MATLAB, Natick, MA, USA) to minimize the sum of the residual errors for a pair of linear plots linked at one end. The optimization returns the optimal placement of the inflection point, which is the link between the two regressions. The optimization was stopped for a VAF % for both curves, otherwise an additional linear plot was introduced with another linkage. This routine was repeated until the VAF reached 95% or greater for all the curves. For all of the

data tested we found only one inflection point and two passive stiffnesses. We chose to fit linear regressions in the analysis of passive stiffness because our protocol seeks to measure the quasi-static stiffness of the SATM complex. 2) Reflex Threshold Calculation (Force and EMG): The reflex threshold is defined as the indentation position at which reflex responses of the biceps brachii to the small taps can be recorded consistently, using either SATM complex force or biceps EMG. The reflex threshold estimate is based solely on the indentation position read from the micrometer of the device (Fig. 1) for a 1 mm sharp tap and should not be equated with other types of thresholds such as motoneuron pool threshold or motoneuron action potential threshold. To estimate this indentation threshold we employ a permutation method based on the statistical bootstrapping method [43]. First, we determine if each of the post-stimulus values is above the mean value, plus three times the standard deviation of the pre stimulus values. In the event that the post-stimulus value is greater, a binary value of 1 is given to that post-stimulus value otherwise, it is set at 0. The result of this first step is an matrix of binary values, where is the number of taps (five in our case) and where is the indentation position (up to 30 in our case). Second, we permute the matrix along the direction to give us a matrix of binary values. Each row of this matrix represents a possible response scenario from the stimuli as the indentation position increases along the direction. Finally, for each row of the matrix of binary values we search in the direction, for the first value or indentation position, at which all the values subsequent to first n value are 1. This search returns a vector of indentation positions. From this vector we calculate the reflex threshold by taking its mean as well as its standard deviation. 3) Reflex Stiffness Calculation: The reflex stiffness of the SATM complex was estimated from the slope of the regression line of the maximum reflex force/indentation position curve. The regressions were performed only on the data that had active reflex responses (i.e., a response which was above the reflex threshold). 4) Side to Side Comparison: Affected Versus Contralateral: Passive Stiffness: We developed a method to compare the passive stiffnesses (as estimated from the slopes of the preload force/indentation position curve) of the two sides in each stroke survivor. Using the inflection point calculated above, we split the preload data into two groups for each subject; Below Inflection Preload (BIP) data and Above Inflection Preload (AIP) data. We removed the offsets from each group, so that they were centered at the origin, because we were interested in comparing the slopes. We then matched each BIP and AIP from the sides of each stroke subject, and subtracted them from each other. Finally, we performed a linear regression on the differences. With this method, we expect that similar stiffnesses will show a regression fit that is not different from 0 within %. Reflex Threshold: We compared the reflex threshold from the affected and contralateral side of each subject with a pairedsample t-test within 5%.

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III. RESULTS The objective of our study was to develop a device and an application protocol that was able to more accurately quantify the DTR by varying the indentation depth of the tested SATM complex. Unlike other methods, this device used a new approach in which the tendon was preloaded (“pre stretched”) prior to being tapped. This allowed for the exploration of a wider range of initial conditions of the SATM complex, which was shown to be important in the measurement of spasticity. From our measurements (force at the tendon and EMG at the muscle), we extracted two main results: first we recorded the effect of progressive indentation on the passive SATM complex [Fig. 3—Phase (I)], and second, we recorded the effect of indentation on the reflex response subsequent to the tap [Fig. 3—Phase (III)]. A. Effect of Indentation Position on Passive Stiffness The resistive force (passive stiffness) on both sides increased with increasing indentation position in all stroke survivors. For each of the preload force measures, no muscle activity was recorded from the surface EMG signals. A single inflection point was found for the passive stiffness curves on both sides of the subjects. This underlines the observation that for the indentation range tested, the SATM complex had two distinct stiffness values. Out of the nine subjects, six (6/9) had their inflection point at a lower indentation depth on the affected side compared to the contralateral side. To compare the stiffness values of the affected and contralateral sides, we fit a regression line to the difference of the data recorded below and above the inflection points (see Section II-D2). Virtually all the regression fits produced slopes that were significantly greater than zero (except for one) underlining that the side specific stiffness values are statistically different from each other. The differences in magnitudes of slopes below the inflection points show a different trend. 4/9 of the subjects have a slope difference that is very close to zero while 5/9 have a slope difference at least 20% greater than zero. This trend is illustrated in Fig. 4(A) for two subjects, who are representative of each trend. Thus the population below the inflection point splits into two groups: one group that has similar stiffnesses and a group that does not. The differences in magnitudes of the slopes above the inflection points are all similar, with one exception. 8/9 of the subjects show a difference in slopes of at least 25%. Except for one subject, we found that the slopes of the affected sides are greater than the contralateral above the inflection point. B. Effect of Indentation Position on Reflex Response The maximum reflex transient force is a global measure of the reflex response of the SATM complex. A primary objective of our study was to characterize the biceps reflex response as a function of indentation depth. In all of our subjects we were able to measure a definitive indentation depth threshold for the biceps’ reflex response. Further indentation after a measureable reflex response resulted in an increased response in both the EMG and force. Unlike the passive stiffness results, the effect of the indentation position on the reflex response was similar for all nine

Fig. 4. Force and EMG results from the SATM complex from two study particiresults as a function of indentation position. The pants. (A) Preload force preload force values originate from the affected side (red filled circles) and from their contralateral side (blue open circles). The slope of the preload force/indentation position curve is a measure of the passive stiffness of the SATM complex. Each of the participants show an inflection point on the slope for both sides tested showing that the SATM complex has two different types of passive stiffas a function of the indentation position. The nesses. (B) Reflex force values originate from the affected sided (red filled circles) and from the contralateral side (blue open circles) of the subjects. The reflex thresholds of each participant are shown for both sides if one exists. The reflex threshold of all the participants was lower on the affected side. The slope of the reflex force/indentation position curve, post the reflex threshold, represents the reflex stiffness of the side tested. All participants show a stiffer reflex response on their affected side compared to their contralateral side. (C and D) RIEMG of the medial and lateral biceps as a function of indentation position. The RIEMG plots show reflex thresholds of both sides if one exists. The reflex threshold of all participants was lower on the affected side. The RIEMG plateaus as the indentation position is increased.

subjects. All subjects had a greater reflex stiffness on their affected side compared to their contralateral side. These responses

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IV. DISCUSSION A. Discussion: Indentation Effect on Passive Stiffness

Fig. 5. Relationship between the MAS and the Normalized Affected Reflex Threshold calculated from the SATM complex force, the biceps lateral and the biceps medial results. The reflex threshold is normalized to the maximum indentation depth attained for each subject.

also trend upwards as the indentation depth increases in a linear fashion % . The slope of this trend is a measure of “reflex stiffness” of the tested SATM complex. This trend is paralleled by the EMG measured at the biceps muscle [Fig. 4(C) and (D)]. Unlike the force measurements, the EMG response plateaus at the deepest indentation levels for all subjects on both sides. The indentation position also affects the position of the reflex threshold, defined as the indentation position at which a consistent reflex response is measured. For 9/9 of our subjects, the reflex threshold was lower on the affected side compared to the contralateral side using the force measure . For 9/9 of our subjects, the reflex threshold was also lower on the affected side compared to the contralateral side using the EMG from the lateral and medial biceps . Finally, the reflex threshold was measured to be lower using the force at the tendon 15/18 for the biceps lateral measures and 14/18 for the biceps medial measures . C. Modified Ashworth Scale Versus Normalized Reflex Threshold We compared the MAS with the normalized reflex threshold of the affected side of our subjects. The linear relationship between the MAS and the normalized reflex threshold is: for force, for biceps lateral and for the biceps medial (Fig. 5). The relationship between the MAS and the normalized reflex threshold is also negative for all measures (Fig. 5). This suggests that the reflex threshold could be used as a measure of spasticity as a lower MAS score will produce a deeper reflex threshold. MAS showed thus far no clear correlations with other measures.

Larger passive stiffnesses have been previously reported on the affected side of hemiplegic patients when compared to their contralateral side. Those experimental procedures involved slowly stretching a muscle around its joint [38], [44] or using system identification techniques [45], [46]. The increase in passive stiffness has also been recorded in both the upper limb at the wrist [44], [45] and the lower limb at the ankle [38], [46] when compared to both nonparetic limbs, and in control subjects. In each of these studies the limbs were rotated, thus the passive stiffness was measured over the length tension curve of the muscles, in other words, over a range of initial conditions. The larger passive stiffness recorded on the affected side using our device thus follows the trends observed in these studies. It further indicates that our device and method (i.e., indenting the tendon) explores different initial conditions of the SATM complex and could potentially be used to estimate passive stiffness of muscles. The act of indenting the SATM complex is clearly different than rotating a joint. Indentation applies a displacement perpendicular to the natural motion of the muscle while joint rotation is physiologically natural and extends the muscle along its axis. Nonetheless, the trend observed by these passive stiffness results suggests that the indentation method may be broadly similar to the joint rotation techniques previously developed to measure passive stiffness [38], [44], at least over a finite range of indentations. At this point it is difficult to establish a precise equivalency between the two methods without stronger physiological data. Suitable data can however be obtained readily with an imaging study using a modality such as ultrasound in which one could compare muscle length changes under both stretching modalities. (Such a study is currently underway in our group.) Identifying which part of the SATM complex is stiffer on the affected side is not feasible at present with our technique. However, we can potentially explore the passive stiffness of the SATM complex and correlate the findings with measures of muscle mechanical properties using modalities such as ultrasound [47], [48] or MRI [49]. Such a study should help with understanding the physiological changes measured at the SATM complex. To determine the accuracy and repeatability of this indentation method, we still need to perform a sensitivity analysis across a larger population, and over a range of limb positions and indentation angles. In this report, we only focus on nine subjects who were all placed in a similar position and had their SATM complex indented with a similar incidence angle. Even though the current results show striking trends, it is necessary that we explore the limits of this method in the future. In spite of these limitations, the indentation technique offers three novel features. The first is that the equipment needed for this technique is much smaller than the devices designed to measure whole joint forces and torques. This is especially important in a clinical setting, where ease of use, device weight and cost are all concerns. The second novel feature is that our technique is able to target a single SATM complex. This is particularly interesting because, unlike the studies using joint rotation, our

CHARDON et al.: QUANTIFYING THE DEEP TENDON REFLEX USING VARYING TENDON INDENTATION DEPTHS: APPLICATIONS TO SPASTICITY

method is less likely to recruit afferents from other muscles, skin and connective tissue, thus giving a more directed measure. Finally, the passive stiffness values measured at the SATM complex using this technique could reflect muscle architecture changes. This could be particularly helpful in diagnosing and treating people suffering from muscle pathologies such as spasticity, whose muscle architecture has been shown to change significantly [51]. B. Indentation Effect on Reflex Response Larger reflex stiffnesses have also previously been reported on the affected side of stroke survivors. The techniques used in earlier studies ranged from large joint rotation [44], [51], [52], ballistic tendon taps [38] to system identification techniques , [45], [46]. Our results are in line with these previous works. Reflex thresholds also have previously been reported in literature as a surrogate measure of spasticity; the earlier a threshold is detected, the more spastic the tested muscle. The technique used previously again required large joint rotations at the elbow with significant velocities [51], [52]. The reflex threshold was the angular position at which the elbow stiffness rose above baseline in conjunction with biceps EMG activity. These earlier studies also found that the joint angle at which a reflex threshold was recorded was always smaller on the affected side. On a similar note, this threshold phenomenon was also reported using a systems identification protocol [45] in which the subjects’ arms were rotated rapidly about a given joint (such as the elbow). In this experiment it was shown that the muscle had a maximum reflex response gain for a given angle of the elbow. Our results further support the view that the indentation of the SATM complex is broadly equivalent to stretch of the muscle by a rotation. Even though the input modalities are different, the effect of the indentation position seems to resemble the effect of a joint rotation on the reflex response and thus this device has the potential to be used to measure the level of spasticity of individuals. In order to establish the overall accuracy and repeatability of the reflex assessment of the SATM complex response, a larger population and a range of patient positions and indentation angles should be tested. In addition, the reflex portion of the SATM complex response is also dependent on the biomechanics of the SATM complex since the SATM complex will ultimately influence the strain that the spindle is subjected to. In order to truly control the input strain onto the spindle, we should theoretically have an estimate of the various stiffnesses of the different parts of the SATM complex. Thus far, this and earlier studies have not taken the SATM complex’s biomechanics into consideration, perhaps because microelectrode studies have shown that spindle afferents respond similarly prior and post-stroke [53]–[56] or because the stiffness measurements are difficult to make in vivo and are still inconclusive [57]–[60]. C. Effect of Controller Saturation on Measurements The controller saturation only affected the performance of the transient taps at high load values ( N). For the static load measurements, however, the controller was able to sustain the command position for all loads tested. Therefore, the passive force results are not affected by controller saturation.

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Even though the reflex portion of our results could be affected for heavy loads, the majority of the reflex data lies below 14 N. In 7/9 of our subjects, the preload values never went above 14 N for the contralateral side and in 5/9 of our subjects for the affected side. If we focus on the sides of the subjects that did have preloads above 14 N, the worst-case scenario shows forces above 14 N for just 10% of the data on the contralateral side and 15% of the data for the affected side. It is thus safe to conclude that the reflex thresholds as well as the initial gain results were not affected by the controller saturation for this subject population, because these values were recorded at preload values well below 14 N. Finally, the reflex responses continue to increase even for heavy loads as observed on the reflex force plots [Fig. 4(B)]. This suggests that the device was able to perform adequately even under heavy loads. If the stimulus was poor at high loads, we should have seen a decrease of the reflex response. Nevertheless, improvements can be made. We are planning to increase power to the controller and are exploring alternative control schemes. Furthermore, from this series of experiments we now believe that it is not necessary to reach heavy loads to obtain our results. D. Force Measure Versus EMG Measure Our results also suggest that the force measures of the SATM complex might be as good as or better than EMG measures. First, to support this assertion, the reflex threshold results were broadly similar, using either force or the EMG. The force measure was actually more precise 15/18 times against the biceps lateral measures and 14/18 times against the biceps medial measures. Second, the force measure can also provide passive mechanical values of the tested tissues. As we have shown, the passive mechanics of the subjects are not similar between sides and between subjects. This information could potentially be used to evaluate the general health of a SATM complex. Third, the EMG values plateau for large indentation positions. We believe that this is most likely due to the saturation of signals in the muscle fibers underneath the EMG electrodes. There comes an indentation position at which all the muscle fibers that the electrode can measure are activated. The EMG electrode will therefore miss reflex response information where the force measure will not [Fig. 4(B) versus Fig. 4(C) and (D)]. Finally, force assessment is relatively cheap and fast. The examiner does not need to prep the skin or purchase advanced filter amplifiers or electrodes to measure the reflex activity from a muscle using force at the tendon. E. Modified Ashworth Scale Versus Normalized Reflex Threshold The fairly strong relationship between the MAS scores and the normalized reflex threshold underlines that threshold estimates using this method are clinically meaningful in that there is an orderly and appropriate relation between the MAS score and the reflex threshold as measured from the indentation depth. However, we believe that this result should be interpreted cautiously for several reasons. First, the MAS has been widely

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shown to be rater-dependent and subjective [10], [61]. To strengthen our results we would need to test many more subjects, across different raters. Second, a relationship could not be established with the contralateral limb because they were all rated with a zero MAS response. We do show that a reflex threshold exists on the contralateral limb of our subject population. Thus, there is a fundamental disconnect between our results and the MAS. Finally, there seems to be overlap in the reflex threshold values with respect to the MAS scores (Fig. 5). This underlines the inherently poor MAS intra-rater reliability and perhaps the lack of resolution of the MAS scale. Because the reflex threshold is unbiased by a predetermined scale, it might expend our ability to quantify spasticity. V. CONCLUSION The DTR is used routinely as a first-line diagnostic tool for many neurological conditions such as spasticity. Its usual configuration is constrained by limited precision, because many parameters are not readily controlled in the course of tapping with a standard hammer. We have shown here that with a novel tendon-tapping device, it is possible to systematically explore the SATM complex of spastic stroke survivors, for the biceps SATM complex, at the least. In addition, to correlate with the MAS scale, our new method is able to extract both the passive and active portion of the reflex response in the values of the passive stiffness, the reflex threshold and the reflex stiffness which are becoming the best empirical values advocated for in the measurement of spasticity [38], [44]–[46], [51], [52]. Furthermore, these values were measured using a device substantially smaller than anything published so far, and has thus a large potential for possible clinical use. A physiological analysis of the mechanisms associated with preloading the SATM complex remains to be accomplished, as well as a sensitivity analysis of the protocol. ACKNOWLEDGMENT The authors thank J. Madoff for her technical assistance and D. Varoqui for her helpful edits. REFERENCES [1] C. Watkins, M. Leathley, J. Gregson, A. Moore, T. Smith, and A. Sharma, “Prevalence of spasticity post stroke,” Clin. Rehabil., vol. 16, no. 5, pp. 515–522, Aug. 2002. [2] P. Urban, T. Wolf, M. Uebele, J. Marx, T. Vogt, T. Bauermann, C. Weibrich, P. Stoeter, G. Vucurevic, A. Schneider, and J. Wissel, “Occurence and clinical predictors of spasticity after ischemic stroke,” Stroke, vol. 41, no. 9, pp. 2016–2020, Sept. 2010. [3] D. K. Sommerfeld, E. Eek, A.-K. Svensson, L. W. Holmqvist, and M. H. von Arbin, “Spasticity after stroke: Its occurrence and association with motor impairments and activity limitations,” Stroke, vol. 35, no. 1, pp. 134–139, Jan. 2004. [4] K. H. Kong, J. Lee, and K. S. Chua, “Occurrence and temporal evolution of upper limb spasticity in stroke patients admitted to a rehabilitation unit,” Arch. Phys. Med. Rehabil., vol. 93, no. 1, pp. 143–148, Jan. 2012. [5] J. W. Lance, R. G. Feldman, R. R. Young, and W. P. Koella, in Symp. Synopsis, Chicago, IL, 1980, pp. 485–494. [6] R. T. Katz and W. Z. Rymer, “Spastic hypertonia: Mechanisms and measurement,” Arch. Phys. Med. Rehabil., vol. 70, no. 2, pp. 144–155, 1989.

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stroke induced spastic quantify spasticity.

Matthieu Chardon received the B.S. and M.S. degrees in mechanical engineering from Northwestern University, Evanston, IL, USA. He is currently a Ph.D. candidate in biomedical engineering at Northwestern University under the guidance of Dr. Rymer at the Rehabilitation Institute of Chicago, Chicago, IL, USA. His interests range from the design and control of collaborative robots (cobots), neural control of movement, to medical and consumer product development. He is now focused on estimating the properties of motoneurons, as well as the development of devices to

William Zev Rymer received the medical degree from Melbourne University, Melbourne, Australia, and the Ph.D. degree in neurophysiology from Monash University, Melbourne, Australia. He is currently researching regulation of movement in normal and neurologically disordered human subjects including sources of altered motoneuronal behavior in hemispheric stroke survivors, using electro-physiological, pharmacological, and biomechanical techniques. As Vice President for Research at the Rehabilitation Institute of Chicago (RIC), he oversees all research endeavors throughout the RIC system of care. He also serves as RIC’s John G. Searle Chair in Rehabilitation Research and Director of the Sensory Motor Performance Program, a position he has held since 1987. In addition to his research roles at RIC, he holds appointments as Professor of Physiology and Biomedical Engineering at the Northwestern University Feinberg School of Medicine. His laboratory receives support from the National Institutes of Health, the Department of Education’s National Institute on Disability and Rehabilitation Research (NIDRR), and a number of research-oriented foundations. After postdoctoral training at the National Institutes of Health and Johns Hopkins University Medical School, he became an Assistant Professor of Neurosurgery and Physiology at the State University of New York, Syracuse, NY, USA. In 1978, he came to Chicago as an Assistant Professor of Physiology at the Feinberg School of Medicine at Northwestern University, and he remained as a primary faculty member in Physiology until his appointment at the RIC.

Nina Suresh received the B.S. degree in computer science and mathematics and the Ph.D. degree in biomedical engineering from the University of Illinois at Chicago, Chicago, IL, USA. She is currently a Research Scientist with the Rehabilitation Institute of Chicago (RIC), Chicago, IL, USA. Her research interests include motor unit firing patterns in stroke, system identification of motoneuron properties in stroke, as well as the characterization of task dependent differences in motor unit firing patterns.