Selective Muscle Activation Following Electrical Stimulation of the Collateral Ligaments of the Human Knee Joint

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1 75 Selectve Muscle Actvaton Followng Electrcal Stmulaton of the Collateral Lgaments of the Human Knee Jont Anthony W. Km, MS, Adam M. Rosen, MD, Vctora A. Brander, MD, Thomas S. Buchanan, PhD ABSTRACT. Km AW, Rosen AM, Brander VA, Buchanan TS. Selectve muscle actvaton followng electrcal stmulaton of the collateral lgaments of the human knee jont. Arch Phys Med Rehabl 1995;76:75-7. The objectve of ths study was to establsh the presence of a local neurosensory reflex arc from mechanoreceptors n human collateral lgaments and jont capsule to knee muscles and to determne f these muscles could be selectvely actvated as varus or vagus stablzers usng randomzed trals. All studes were performed n the research department laboratores. Eleven subjects were recruted from the unversty staff and students based on no pror hstory of knee alments. Subjects lad supne on an expermentaton table as a current-modulated electrcal stmulaton was provded through the medal (MCL) or lateral collateral (LCL) knee lgaments. Latency of actvaton was measured for seven muscles, four by surface electrodes (semtendnosus, bceps femors long head, vastus medals, and laterals), and three by ntramuscular electrodes (sartorus, gracls, tensor fasca lata). In the protocol, selectve actvaton was defned as the relatve ncrease n the actvty of four muscles wth medal moment arms followng MCL stmulaton compared wth correspondng actvty followng LCL stmulaton. For lateral muscles, the opposte was assumed (e, that more actvty would follow LCL than MCL stmulaton). Monte Carlo smulatons were performed on the data to determne sgnfcant selectve muscle actvaton (p <.5). Statstcally sgnfcant ncreases n actvaton were observed, most consstently, n the vastus medals followng MCL stmulaton and n the vastus laterals followng LCL stmulaton. These results suggest that a neurosensory reflex arc from lgament mechanoreceptors may provde varus and vagus stablzaton and knee muscles may be selectvely actvated to counter varus or valgus loads by the Amercan Congress of Rehabltaton Medcne and the Amercan Academy of Physcal Medcne and Rehabltaton The uncondylar degeneraton typcally assocated wth osteoarthrts of the knee has been attrbuted to the nadequate performance of the knee stablzng mechansms durng varns or valgus loadng.~'2 It has long been accepted that lgaments are necessary passve bomechancal stablzers of the knee jont. Cadaver studes have delneated the quanttatve and qualtatve propertes of the crncate and collateral lgaments n knee stablzaton. Recently however, attenton has been pad to the neurologcal role that sensory organs n lgaments and muscles play to ensure knee jont stablty. Ths observaton was frst made n the late 195s by Stener and hs colleagues who hypotheszed that lgaments play a protectve reflexve role n stablzng the knee. 3-6 However, as these studes were unsuccessful n delneatng sources of reflexve muscle actvty, research n ths partcular area dmnshed. Recently, several dfferent types of mechanoreceptors have been dentfed n human and anmal knee crncate lgaments, collateral lgaments, and the mensc. 7-~j Zmny ~2 has descrbed four type of mechanoreceptors found n both From the Department of Physcal Medcne & Rehabltaton (Drs. Brander, Buchanan), Department of Medcne (Dr. Rosen), Dvson of Arthrts and Connectve Tssue Dseases, Northwestern Unversty Medcal School, and Sensory Motor Performance Program (Mr. Km, Dr. Buchanan), Rehabltaton Insttute of Chcago, IL. Submtted for publcaton July 29, Accepted n revsed form January 18, Supported n part by the Ralph and Maron C. Falk Medcal Research Trust. No commercal party havng a drect fnancal nterest n the results of the research supportng ths artcle has or wll confer a beneft upon the authors or upon any organzatons wth whch the authors are assocated. Reprnt requests to Thomas S. Buchanan, PhD, Sensory Motor Performance Program, Room 146, Rehabltaton Insttute of Chcago (M/C E89), 345 E. Superor St, Chcago, IL by the Amercan Congress of Rehabltaton Medcne and the Amercan Academy of Physcal Medcne and Rehabltaton /95/ / capsular lgaments and mensc. She calls them type I (Ruffn), type II (Pacn), type III (Golg), and type IV (free nerve endngs). Pacnan corpuscles, because of the nature of ther hghly transent responses, are nvolved n acceleratons, quck movements, and vbratons. Ruffn endngs provde contnuous or tonc reflex regulaton over muscle tone. Golg tendon organs dscharge to sgnal tenson, jont poston, and drecton of movement at the extreme degrees of jont dsplacement only. The presence of these mechanoreceptors rases questons of how they act as neuromuscular elements. Drect a-motoneuron actvaton from lgamentous! capsular stmulaton has been typcally assumed to be the mode by whch the sensory afferent nformaton traveled to produce reflexes, t3-18 Indrect fusmotor actvaton has also been suspected as beng the prmary neuromuscular mode of reflex actvaton.~9 Regardless of the mode of afferent-drected muscle actvaton, the overall response of the muscles s most lkely amed toward ensurng that the jont remans ntact. Ths goal may be acheved through actvaton of specfc muscles, eg, those wth moment arms that allow them to most effectvely oppose varus or valgus loads. Ths selectve actvaton may be the result of a prevously traned and learned muscle actvaton pattern that, n healthy subjects, s a functon of the ongong afferent nformaton provded by the sensory receptors of the knee jont. Ths pattern may be a delberate mechansm by whch the knee jont s stablzed to counteract ncreased uncondylar forces produced by malalgnments of the knee that promote jont degeneraton. It has been proposed that the loss or change n sensory feedback from lgament njury may result n devatons from typcal muscle actvaton patterns, whch n turn may lead to undesrable changes n jont stablty. ~9 These detrmental changes n

2 ELECTRICAL STIMULATION OF THE KNEE COLLATERAL LIGAMENTS, Km 751 jont stablty may have a consderable effect n promotng jont degeneraton. It was found that dogs that underwent medal collateral lgament (MCL) removal as well as specfc nerve transectons were more lkely to develop osteoarthrts than those wth the MCL removed but wthout nerve transecton. 2 Other studes usng rabbts showed that when the anteror and posteror crucate lgaments (ACL and PCL, respectvely) and the MCL were transected, osteoarthrtc changes were accelerated followng repettve jont loadng. 2L In addton, people who suffer from dabetes melltus, leprosy, and tabes dorsals (condtons known to cause neurologcal defects) develop Charcot's arthropathy. It s generally beleved that nonspecfc loss of sensory nformaton seems to accelerate jont degeneraton. Many of the knee jont muscles could voluntarly or reflexvely contrbute to stablzng the knee durng varus or valgus loadng. However, there s no evdence n the lterature showng that neuromuscular system actvty s related to varus-valgus stablty or loadng. There s also no evdence showng that cocontracton or specfc actvaton of the knee muscles s used to stablze the jont. Ths nvestgaton was desgned to ascertan whether muscles are reflexvely nvolved n the support of smulated varus or valgus loads. The hypothess of ths nvestgaton was that by provdng electrcal stmulaton to the MCL and LCL of the knee smulatng a valgus and varus stretch, respectvely, receptor actvty would be nduced. The excted receptor actvty would then result n stablzng muscle actvty, va spnal reflexes, n the medal or lateral muscles about the knee. These reflexes would be manfest as heghtened EMG actvty n the muscles pslateral to the lgament stmulated. The presence of muscle actvty followng the stmulaton would be ndcatve of a motor control system that s aware of varus or valgus loadng condtons and that manfests tself n selectve muscle actvatons that act to stablze the jont n response to such loads. METHODS Preparaton Eleven healthy subjects (2 women, 9 men), wthout pror hstory of knee njury, arthrts, hstory or clncal exam suggestve of mechancal derangement, were tested. The age range of the subjects was from 24 to 47 years. EMGs were recorded from the followng muscles: the sartorus (SR), gracls (GR), vastus medals (VM), vastus laterals (VL), semtendnosus (ST), bceps femors long head (BFL), and tensor fascae latae (TFL). Electromyographc sgnals from the SR, GR, and TFL were recorded usng pars of fne-wre ntramuscular electrodes (75-mcron dameter Teflon-coated stanless steel wres, nserted usng 27-gauge hypodermc needles) placed approxmately 2cm apart. The remander of the muscles, whch are larger and more superfcal, were examned usng surface electrodes (Medtronc no pedatrc electrocardogram [ECG] electrodes wth a 14mm dameter surface gel). Preceedng the placement of the surface electrodes, the skn was mldly abraded and then cleansed wth an alcohol wpe. Electrode placement followed that advsed by Perotto 22 and was verfed usng standard muscle testng procedures. 23 Two addtonal pars of surface electrodes were placed over the mddle porton of the quadrceps and hamstrngs to record nonspecfc knee flexor and extensor actvty for use n the target matchng protocol (see below and fg 1). Stmulaton electrode pars were placed n four locatons: the MCL, the LCL, and on the skn slghtly dstal to the MCL and LCL. The ntralgamentous MCL and LCL electrodes were mplanted usng fne-wre electrodes and were roughly 2cm apart, near the nsertons of the lgaments. Lgaments were localzed by palpaton and knowledge of the bony landmarks. Placement of the electrodes was always performed by one expermenter to mnmze varatons n placement. The thrd and fourth pars of electrodes served as controls and were placed on the skn usng surface electrodes wth the purpose of stmulatng cutaneous receptors. The MCL and LCL were stmulated usng current-modulated pulse trans. The pulse tran characterstcs used were based on a plot study amed at determnng the pulse frequences, pulse tran duratons and current ampltudes that would elct the greatest actvty. In ths study, 5ms undrectonal rectangular pulses actvated n 5Hz pulse trans were used, as these were determned to yeld the greatest reflex response. These pulse trans were actvated for a tran duraton of 45ms (resultng n three pulses) (fg 1). The polarty of the pulse was changed every 3 or 4 trals to mnmze capactance buld-up on the electrodes. For each subject, the current level was adjusted before data collecton to attan subpan threshold levels. The resultant current range was :4 to.8ma. Every tral conssted of a looms restng perod followed by the three current pulses, lastng a total of 5ms. Protocol To ensure that any reflexes that occurred would be greater than the threshold level of actvaton, a constant background level of muscle actvty was mantaned throughout the experment. Ths was done by usng a target matchng protocol. In ths protocol, the root-mean-squared (RMS) EMGs from the two electrodes that were placed on the quadrceps and hamstrngs were dsplayed on a computer screen n real tme n the form of a sngle cursor. The sgnal from the quadrceps was used to determne the y-coordnate of a cursor, and the sgnal from the hamstrngs determned the x-coordnate. Subjects were asked to vew the computer montor and place the crcular cursor (drven by the EMG sgnals) nsde a statonary larger target crcle dsplayed on the screen. The target crcle was postoned to represent equal contrbutons from flexors and extensors at approxmately 3% of maxmum. Before data acquston, subjects practced the target matchng procedure untl they reached a level of performance where they could quckly and accurately perform ths task. Durng the actual experments, data acquston was started after the cursor was n the target regon. Data were collected for 5ms and the electrcal stmulaton was appled looms after the ntaton of data collecton. Muscle Categorzaton Muscles were categorzed as beng ether medal or lateral muscles, dependng on whether they had medal or lateral

3 752 ELECTRICAL STIMULATION OF THE KNEE COLLATERAL LIGAMENTS, Km Target Matchng ~/" Montor / I Cursor ( ~ HM RMS EMG Q Target 5)! I I I 5 I 6 ms \ Current Pulse Tran 2 ms 4 ms \\\ \\\ \ \ / Femur / // /PCL Intralgamentous ~k~~ll Electrodes ~ ~ )/~ nmcl f '~Tba,~y I \ [I {Fbula Fg 1--Overvew of the expermental set-up. Once the subject was secured on the examnng table he was drected to perform the target matchng protocol. When the prerequste amount of background muscle actvty was produced by the subject, the stmulaton was appled. The resultant EMGs were collected for off-lne analyss. moment arms (fg 2). A bomechancal model of the knee based on that reported by Delp and coworkers 24 was used to determne the potental contrbutons of each muscle. 25 Ths model used dgtzed bone geometry and reported values for muscle attachment stes to determne muscle paths. It shows that when the knee s at full extenson several muscles have consderable medal or lateral moment arms n addton to ther flexon or extenson moment arms. In ths model, t was assumed that varus rotatons occurred about the medal condyle and valgus rotatons occurred about the lateral condyle. In general, each muscle had ether a medal or lateral moment arm regardless of whether the rotaton center was assumed to be under the medal or lateral condyle. The exceptons to ths case were the vastus medals and vastus laterals. Despte the classfcaton of the VM and VL as medal and lateral muscles, they could have both opposed varus and valgus moments because they had a common nserton ste on the patella. However, both the VM and VL have other nsertons nto the knee capsule, and possbly nto the collateral lgaments. 26 Hence, t may be possble that the true resultant moment arms for the VM and VL were more medal and lateral, respectvely, than ndcated n fgure 2. Subsequently, we classfed the VM and VL as beng medal and lateral muscles, respectvely. The ST also had a partal medal moment arm, but ths component was excluded because t was relatvely small. EMG Analyss Durng the experments, EMG sgnals were preamplfed (2dB) and hgh pass fltered (1Hz), then amplfed (2dB) and low pass fltered wth an eghth order Butterworth flter (3Hz). As a part of the set-up procedure, subjects were nstructed to maxmally contract each muscle and the amplfer gan for the correspondng EMG channel was adjusted so that maxmum EMG actvty would be just short of saturatng the amplfers. The EMGs were dgtally sampled at 1, Hz and stored for off-lne analyss. Followng the experment, the dgtzed EMG sgnals were frst rectfed and smoothed and then separated nto two groups of approxmately 8 to 12 trals each, based on whether they were recorded durng the LCL or MCL stmulatons. From each muscle's EMG sgnal the baselne average, EMGb~sej~ne (measured n volts), and standard devaton were determned from the values n a 9ms wndow before the stmulaton. From the same sgnal a perod of reflex actvty was found and averaged to obtan EMQctve. For each muscle, the EMGbase~,e was then subtracted from the EMGactve for each of the MCL stmulaton trals and these dfferences were averaged to gve the EMGrenex measure (equaton 1). The same procedure was used to produce EMGre~cx measures from the LCL stmulaton trals. For each muscle, the EM- Greflex values for the LCL and MCL stmulatons were then compared to see n whch drecton the hgher actvty occurred. N (EMGactve - EMGbaselne) EMGre~l~x = = J (1) N where N s the number of trals. A custom program was wrtten, usng a statstcally based method, to solate the perod of reflex actvty from the EMG sgnals. A peak of actvty was searched for n a 4 to 175ms wndow after the start of the stmulaton. When ths peak was found, the burst onset was dentfed by movng backwards n tme and stoppng when three consecutve data ponts wthn three standard devatons from the baselne actvty were found. Smlarly, the end of the EMG burst was dentfed

4 ELECTRICAL STIMULATION OF THE KNEE COLLATERAL LIGAMENTS, Km 753 TFL F, Extenson 1-,- VL Lateral I I I [ I -1 BFL " _L VM r~l r! o ST SR,,_-,, Medal,, 1-1 Flexon Fg 2--Moment arms of selected knee muscles wth the knee fully extended (cm). Ths plot shows the moment arm postons n the fexon-extenson-varus-valgus plane. Moment arms are drawn as lnes because the center of rotaton for varus-valgus moton s not fxed. It shfts from beneath the medal to beneath the lateral condyle of the humerous and the muscle moment arms shft accordngly. The boxes correspond to moment arms determned relatve to the medal condyle and crcles correspond to those determned relatve to the lateral condyle. Flled symbols correspond to the moment arms for whch each muscle would have the greatest mechancal advantage. Note that at ths jont angle all muscles have sgnfcant varus-valgus moment arms relatve to ther flexon-extenson moment arms. The data n ths fgure were generated by the model of Lloyd and Buchanan. 2~ by travelng forward n tme. The use of three standard devatons and three data ponts was thought to be suffcent to dentfy the true reflex onset and offset and not just random actvty. The 4ms start of ths range was chosen because most actvty before ths tme would most lkely not be from reflexes, but rather movement artfact. The 175ms end of ths range was chosen because the ntermedate spnal reflexes have been reported to end approxmately at ths tme. 27 A fxed tme wndow was not used because the onset tmes and duratons of the reflex responses vared among subjects. We ntally used a rgd tme wndow to determne the reflex response, but croppng or dlutng of mportant spkes of EMG actvty were observed. If no reflex actvty was solated, t was concluded ether that no reflexes were present or that they were bured n the varablty of the data. For those EMG recordngs that yelded muscular reflex actvty, further statstcal tests were conducted to see f the dfferences between the muscle reflexes (EMGren, from LCL and MCL stmulatons were sgnfcantly dfferent. Statstcal analyss was performed usng Monte Carlo smulaton tests where every possble permutaton of par dfferences were calculated and then analyzed. Student's t-tests GR were used to determne f the EMG dfferences were sgnfcantly greater than zero (p <.5). That s, for each muscle of each subject, t tests were used to determne f EMGs sgnfcantly ncreased after electrcal stmulaton of one lgament compared wth stmulaton of the other. Results not satsfyng ths crteron were concluded to show no sgnfcant preferental actvty. To quantfy the magntude of the dfferences n reflex actvtes across subjects, rather than just ndcatng the presence of sgnfcant dfferences, a normalzed EMG value was developed. Equaton 2 shows how ths normalzed value was calculated for the reflex actvty n a lateral muscle. I~]~/[('~=LCL Stm. -- I~'!~/It'~MCL Stm ~*'-vnorm]:~m~latera I = ~'... fl flex (2) EK/W', LCL Stm. lvx~oreflex The normalzed reflex value from a lateral muscle, EMGt,"t*r~!, was determned by takng the dfference between the EMGre,~x from the LCL and MCL stmulatons, and normalzng t through dvson by the LCL stmulaton response. Smlarly, the reflexes from the medal muscles were normalzed, except that EMGr,n,x from the LCL and MCL stmulatons were nterchanged. From ths normalzaton process, all muscles supportng the hypothess would have a rato greater than zero. That s, medal muscles should be more actve followng MCL stmulatons than followng LCL stmulatons, and vce versa for the lateral muscles. Usng ths measure, a sngle value for the magntude for each of the 11 subjects could be presented and more easly evaluated (table 1). Postve values support the hypothess and negatve values oppose t, e, contrary to expected. No actvty (NA) was used to ndcate that there was no dscernble actvty followng the stmulaton, e, no change from background actvty for the reasons mentoned earler and were assgned a numercal value of zero. RESULTS A typcal reflex response followng electrcal stmulaton of a collateral lgament s shown by an ensemble plot of subject 2's ST EMG (fg 3). The ST shows a very pronounced reflex followng the MCL stmulaton and vrtually no response followng the LCL stmulaton. The tmng of Table 1: Normalzed EMG Values Subject SR GR ST VM BFL TFL VL 1 na na na * na.77* 3 na na na na na * " na na * na na na na na na 6 na 1.2 na.66 na na.74 7 na na na 9.35 na na na na.51 na na.57 9 na na na.87* na na na na.99* na Normalzed EMG reflex values for all subjects, calculated usng equaton 2. All values were statstcally sgnfcant (p <.5) except as ndcated by astersk. NA ndcates that no actvty could be detected usng our algorthm. Ths was equvalent to a zero value as t mpled that there was no change n actvty from the background level.

5 754 ELECTRICAL STIMULATION OF THE KNEE COLLATERAL LIGAMENTS, Km A.8 Pulse Pulse 5 ST ST 1 2 Tme (ms) Tme (ms) Fg 3--Electrcal current pulse (ma) and EMG actvty (volts) n the ST muscle assocated wth MCL (A) and LCL (B) stmulatons. Muscle actvty was measured over the tme wndow between cursors 1 and 2, whch were computed as descrbed n the text. A baselne level of actvty was taken for a tme wndow before the stmulaton, as marked by cursors 3 and 4. Note that actvty n the ST (whch crosses the knee on the medal aspect) s sgnfcantly hgher followng the MCL stmulaton. Artfactual actvty was recorded from the EMG elecrodes durng the tme of electrcal stmulaton. the burst of actvty s approxmately 128 to 144 ms after the ntaton of stmulaton, suggestng the presence of strong reflex actvty followng the stmulaton. Every subject showed actvaton n at least one expected muscle followng electrcal stmulaton of the collateral lgaments. The control surface electrode stmulaton revealed no correspondng change n EMG, ndcatng that cutaneous afferents dd not play a role n the EMG recordngs we observed. In the next analyss, responses from all muscles of all CO 6- ~6 E Z SR GR ST VM BFL TFL VL Muscles Fg 4--A comparson of the number of subjects supportng our hypothess (e, that medal muscles wll be actvated sgnfcantly more after MCL stmulatons than LCL stmulatons, and vce versa for lateral muscles). The plot shows, for each muscle, the number of subjects for whom statstcally sgnfcant (/7 <.5) dfferences were observed when usng t-tests to compare these two groups. subjects were Compared usng equaton 2 (fg 4). For the VM, a medal muscle, n 8 out of 11 subjects, EMGreflex from the MCL stmulaton were sgnfcantly greater than EMGrenex from the LCL stmulaton and vce versa for the VL, a lateral muscle, n 6 of 11 subjects. The remanng medal muscles, SR, GR, and ST, showed moderate support wth 4 of 11, 4 of 11, and 5 of 11 sgnfcant dfferences, respectvely. The remanng lateral muscles showed more modest support wth the BFL and TFL exhbtng 3 of 11 and 4 of 11 sgnfcant dfferences, respectvely. The normalzed EMGs were averaged across subjects to measure how much a partcular muscle ncreased ts actvty followng stmulaton of the same-sde lgament as opposed to stmulaton of the opposte-sde lgament (fg 5). The SR, GR, and ST exhbted ratos of approxmately one, one and a half, and two, respectvely, ndcatng a preference toward actvaton durng MCL stmulatons as opposed to durng LCL stmulatons. The VM and BFL exhbted the largest ratos, but also had the largest standard devatons. The TFL and VL, both lateral muscles, had ratos near one, ndcatng less powerful selectve actvaton n ths paradgm. Ths could be explaned by the numerous nactve cases that were computed nto the average as zero. In averagng the normalzed EMG results, values reported as NA were gven a numercal value of zero, whch lowered the averages for these muscles. The ratos for all muscles ranged from approxmately.9 to 2.4, whch corresponds to roughly a 9% to 24% ncrease n reflex actvty when the same-sde lgament was stmulated as opposed to when the opposte-sde lgament was stmulated. On average, the SR was actvated at an earler tme than the other muscles (table 2). The two hamstrng muscles, ST and BFL, were actvated last at approxmately 12 to 13ms. Arch Phys Med Rehab! Vol 76, August 1995

6 ELECTRICAL STIMULATION OF THE KNEE COLLATERAL LIGAMENTS, Km 755 o (.5 uj._n E z I I I I I I I..., t... I I [ I I I I SR GR ST VM BFL TFL VL Muscles Fg 5--Normalzed EMG reflex actvaton ratos computed usng equaton 2 (dmensonless unts). The values reflect the rato by whch the selectvely actvated muscles reacted to the stmulaton n one drecton versus the stmulaton n the opposte drecton. Postve values ndcate that there was reflex actvty n medal muscles after stmulaton of the MCL than LC! (and vce versa for lateral muscles). The GR was actvated n between the latences of the other two pes anserne muscles. Oddly, the onset tmes of the VM and VL were relatvely far apart. Ths result was unexpected as they are vrtually the same n magntude but only dfferent n drecton. The duraton of the reflexes encompasses a narrow range; ST and BFL exhbtng the lower and upper extremes of the range at 7.2 and 5ms, respectvely. DISCUSSION Reflex actvty followng ether MCL or LCL stmulaton ndcated that, n general, muscles were actvated based on ther lateral-medal moment arms. Ths suggests that muscles play a role n stablzng the knee ndependently of ther roles as flexors or extensors. Assumptons and Lmtatons It was assumed that electrcal stmulaton of the collateral knee lgaments actvated the mechancal stretch receptors located wthn the body of the lgaments. Although the MCL les partally wthn the medal jont capsule, stmulaton of the capsule would not lkely result n the drected reflex muscle actvaton that was observed. If jont capsule stmulaton dd occur, t lkely contrbuted only to localzed sensaton and not muscle actvaton. Ths s supported by a plot study where we anaesthetzed the jont capsule by nfusng ldocane nto the knee jont of human subjects and conducted smlar electrcal stmulaton. We observed smlar reflex actvaton patterns as noted n ths study wth the excepton that subjects noted decreased sensaton of electrc shock. Cutaneous afferent sgnallng was ruled out as a possble source of feedback because no reflex actvty was found followng the control surface stmulaton. Subjects consstently noted a sensaton of current spreadng through the knee jont, durng MCL stmulaton. For the LCL stmulaton, they noted a more localzed stmulaton. The dfference n sensory experence may support the noton that capsular mechanoreceptors are actve neural contrbutors to jont stablty. That s, because the MCL s partally ntracapsular, the sensaton of current spreadng felt n the jont may have resulted from current spread throughout capsular receptors. Ths anecdotal result would be n accordance wth several studes also suggestng that capsular receptors, n addton to lgament receptors, are actve neural stablzng elements. In bomechancal cadaver studes, the MCL and ACL work together to stablze the knee aganst excessve valgus moton It could be possble that these two lgaments work synergstcally as neural elements to stablze the knee n excessve valgus moton. Operatng as both passve and actve stablzng elements, these lgaments may serve to sgnal the muscles, such as the VM and VL, to stablze the knee n the presence of consderable bomechancal stresses that the lgaments alone cannot sustan repettvely. The physologcal sgnfcance s that the relatvely good vast muscle responses would seem to support the dea that actvatng the quadrceps may work to stablze the jont even n the varus-valgus plane. 27 Also, t would support the belef that quadrceps rehabltaton and strengthenng s essental followng knee lgament njury. Reflex Actvty Evaluaton Although the exact source of the afferent feedback cannot be determned wth ths protocol, some sources are much more lkely than others. Because the ste of electrcal stmulaton was n the lgaments and not near the spndles of the muscles, muscle spndle sensory afferent actvty should not have played any role n the responses recorded. They also would have acted qucker than the responses observed. Studes of the stretch reflex from muscles spndles (Ia afferents) from the human soleus have latences for ntal phasc bursts n the range of 4ms. 3~ However, reflexes observed n ths study were n the range of approxmately 9 to 13ms (table 2). Another possblty s that the reflexes were not exclusvely spnal reflexes but rather came from hgher centersy However, such reflexes would have onsets near 175ms whch s slower than those observed. Voluntary contractons could Table 2: Reflex Latency and Duraton Averages Reflex Averages SR GR ST VM BFL TFL VL Latency SD 88.4 _ _ _ _ _+_ 28.1 Duraton _+ SD 36.4 _ _ _ _ _ _ _ Reflex latences (onset tmes) and duratons of the actvaton bursts observed n the muscles. For each muscle, the values represent the averages and standard devatons n mllseconds (ms) of all of the subjects tested.

7 756 ELECTRICAL STIMULATION OF THE KNEE COLLATERAL LIGAMENTS, Km have created the spkes of actvty that were observed, however, ths argument can be refuted on two specfc counts. Frst, the onset latences observed would have been too rapd for voluntary responses. Voluntary contracton onset tmes of the knee muscles have been reported to fall nto the range of 215 to 22ms followng mechancally nduced actvty. 27'32 Second, the responses observed were relatvely sharp spkes of actvty, perhaps too sharp to be msconstrued as voluntary contractons. It s mportant to dscount voluntary contractons, especally n the presence of background actvty. Cutaneous receptors mght have played a role n ths reflex. However, because no reflex actvty was found when the stmulaton was appled wth surface electrodes, ths can be ruled out. Capsular responses could also be consdered as possble sources for afferent feedback, partcularly because the capsule has been observed to be nnervated wth sensory receptors (see Introducton). We cannot dfferentate whether the responses were from receptors n the capsule or lgaments, although stmulaton electrode placement would gve preference to those n the lgaments. The latences observed ndcate that the reflexes most lkely orgnate from the stmulaton of artcular mechanoreceptors n the capsule and lgaments, because these structures are nnervated wth sensory receptors possessng slower fber types, 7'8 whch should be actvated n the 9 to 13ms range. Stener 5 was able to produce reflex actvty from drect mechancal lgament stmulaton, but found that n subjects wth lgament ruptures, probng around the lgament provded smlar reflex actvty that ndcated that capsular receptors also play a role n mantanng jont ntegrty. Solomonow and coworkers j8 found that n humans wth ruptured crucate lgaments, there was a hamstrng reflex ndcatng that the receptors n and around the capsules may have played a role n mantanng the knee jont stablty that perhaps the ACL had provded earler. Smply removng the requrement of background muscle actvty was not an opton because t was mportant to ensure that any sensory receptors were near threshold of exctaton. Prevous studes of a smlar nature had shown that no background level of actvty resulted n quescent electromyograms. 5 In fact, when the protocol was frst developed for ths experment, the subjects were not requred to produce background actvty n ther muscles and, as expected, no apprecable reflex EMG actvty was detected. In our study, the reflex responses all occurred after the stmulaton had ceased. In addton, generaton of muscle tenson lags the EMG sgnal. Therefore the muscle tenson, as a result of the reflex EMG, would not occur untl at least llms after the mechancal nsult (allowng 9ms for the reflex loop and 2ms for muscle force generaton). Ths tme delay would be too long for the muscles to provde mmedate protecton to the jont. Rather, the reflexes observed may be part of an adaptve learnng scheme that could be used to establsh a specfc motor pattern to protect the jont and thus to prevent knee jont degeneraton. Knee jont degeneraton n subjects wth varus knee algnment s thought to be caused by large medal compartment loads produced by large knee adducton moments durng the stance phase of gat. 2'33 Noyes and coworkers j showed, however, that some subjects wth varus malalgnment and lgament defcences dd not exhbt these large adducton moments. It may be that these people were able to compensate by reprogrammng ther motor patterns, n the presence of dfferent afferent nformaton from other reflex sources, e, other lgaments or mensc. Moreover, large adducton loads could have been caused by napproprate motor patterns n lgament-mpared subjects. Ths may have resulted n faster jont degeneraton n these subjects. The results of ths study mply that muscles can be reflexvely actvated ndependent of ther roles as flexors or extensors to provde stablty to the human knee durng LCL or MCL stmulatons. The reflex latences suggest that ths selectve muscle actvaton n the varus-valgus plane s not present for the purposes of mmedate stablzaton, but perhaps, for the purposes of adaptng the motor system to stablze the knee n the presence of future smlar destablzng condtons. Further studes are necessary to dentfy the specfc neural elements nvolved. Clncal Relevance Lgaments have commonly been beleved to stablze the knee as passve restrants. Thus, treatment of knee lgament njures tradtonally has conssted of substtutng for these mechancal propertes. Surgcal repar (ether prmary or wth autologous graftng) s often not entrely successful, and patents complan of contnued subjectve feelngs of knee nstablty or pan. It has been proposed that nonsurgcally treated acute lgamentous njures far better than ther surgcally treated cohorts n terms of varous bomechancal propertes. 34 More recent reports, however, contradct ths vew suggestng the possblty of deteroraton of functon over tme, wth ncreased laxty of the secondary restrants. 35 As an alternatve or adjunct to surgcal correcton, knee orthoses are prescrbed. However, many nvestgators beleve that knee orthoses are only margnally effectve n that they nduce actvty lmtatons n ndvduals wth lgament njures and patent complance s varable. Thus, the current strateges for treatment of lgament mparments offer only lmted beneft, perhaps because they address only the bomechancal propertes of lgaments. In summary, we beleve lgament preservaton may have more than just an effect on the mantenance of passve jont stablty, but also on the actve jont stablty provded by lgamento-muscular reflexes, whch have not been prevously shown n humans. If our hypothess s ndeed correct, nadvertent surgcal denervaton of sensory afferents, for example, could result n a destablzed knee predsposed to accelerated degeneratve arthrts. Both operatve and nonoperatve strateges should address preservaton of local sensory afferent nformaton. Rehabltaton regmes amed at neuromuscular retranng may be crtcal to the ultmate outcome. Further nvestgatve research of these types of strateges could lead to specfc rehabltatve nterventons that mprove muscle responsveness to local sensory afferent nformaton, enhancng jont stablty and consequently reducng degeneratve sequelae. Acknowledgment: The authors thank Mr. Paul Trpkovsk, Dr. Davd Lloyd, and Dr. Joseph Gven for ther comments and knd assstance n ths work at ts varous stages. Arch Phys Med Rehab Vol 76, August 1995

8 ELECTRICAL STIMULATION OF THE KNEE COLLATERAL LIGAMENTS, Km 757 References 1. Noyes FR, Schpplen OD, Andracch TP, Saddem SR, Wese M. The anteror crucate lgament-defcent knee wth varus algnment. Am J Sports Med 1992;2: Schpplen OD, Andracch TP. Interacton between actve and passve knee stablzers durng level walkng. J Orthop Res 199l;9: Andersson S, Stener B. Expermental evaluaton of the hypothess of lgamento-muscular protectve reflexes. II. A study n cat usng the medal collateral lgament of the knee jont. Acta Physol Scand 1959;48(Suppl 166): Petersen I, Stener B. Expermental evaluaton of the hypothess of lgamento-muscular protectve reflexes. III. A study n man usng the medal collateral lgament of the knee jont. Acta Physol Scand 1959;48(Suppl 166): Stener B. Expermental evaluaton of the hypothess of lgamento-muscular protectve reflexes: I. A method for adequate stmulaton of tenson receptors n the medal collateral lgament of the knee jont of the cat, and studes of the nnervaton of the lgament. Acta Physol Scand 1959;48(Suppl 166): Stener B, Petersen I. Electromyographc nvestgaton of reflex effects upon stretchng the partally ruptured medal collateral lgament of the knee jont. Acta Chr Scand 1962; 124: Grgg P, Hoffman AH. Propertes of Ruffn afferents n cat knee jont capsule, as revealed by stress analyss of solated sectons of cat knee capsule. J Neurophysol 1982;47: Grgg P, Hoffman AH, Fogarty KE. Propertes of Golg-Mazzon afferents n cat knee jont capsule, as revealed by mechancal studes of solated jont capsule. J Neurophysol 1982;47: Haus J, Halata Z. lnnervaton of the anteror crucate lgament. Int Orthop 199; 14: Schutte MJ, Dabezes EJ, Zmny ML, Happel LT. Neural anatomy of the human anteror crucate lgament. J Bone Jont Surg 1987;69- A: Schultz RA, Mller DC, Kerr CS, Mchel L. Mechanoreceptors n human crucate lgaments. J Bone Jont Surg 1984;66-A: Zmny ML. Mechanoreceptors n artcular tssues. Am J Anat 1988; 182: Ekholm J, Eklund G, Skoglund S. On the reflex effects from the knee jont of the cat. Acta Physol Scand 196;5: Freeman MAR, Wyke B. Artcular contrbutons to lmb muscle reflexes: the effects of partal neurectomy of the knee-jont on postural reflexes. Br J Surg 1966;53: He X, Proske U, Schable H-G, Schmdt RF. Acute nflammaton of the knee jont n the cat alters responses of flexor motoneurons to leg movements. J Neurophysol 1988; 59: les JF, Stokes M, Young A. Reflex actons of knee jont afferents durng contracton of the human quadrceps. Cln Physol 199; 1: Schable H-G, Schmdt RF. Actvaton of groups III and IV sensory unts n medal artcular nerve by local mechancal stmulaton. J Neurophysol 1983;49: Solomonow M, Baratta R, Zhou BH, Shoj H, Bose W, Beck C, et al. The synergstc acton of the anteror crucate lgament and thgh muscles n mantanng jont stablty. Am J Sports Med 1987; 15: Johansson H, Sjolander P, Sojka P. A sensory role for the crucate lgaments. Cln Orthop 1991 ; 268: O'Connor BL, Vsco DM, Brandt KD, Myers SL, Kalasnsk LA. Neurogenc acceleraton of osteoarthross. J Bone Jont Surg 1992;74- A: Lukoschek M, Schaffler MB, Burr DB, Boyd RD, Radn EL. Synoval membrane and cartlage changes n expermental osteoarthrts. J Orthop Res 1988;6: Perotto AO. Anatomcal gude for the electromyographer, 3rd ed. Sprngfeld, (IL): Thomas, Kendall FP, McCreary EK, Provance PG. Muscles testng and functon, 4th ed. Phladelpha: Wllams & Wlkns, Delp SL, Loan P, Hoy MG, Zajac FE, Topp EL, Rosen JM. An nteractve graphcs-based model of the lower extremty to study orthopaedc surgcal procedures. IEEE Trans Bomed Eng 199;37: Lloyd DG, Buchanan TS. Muscle and lgament contrbutons to the support of varus-valgus knee moments determned by bomechancal modelng and expermental data. Proc Am Soc Bomech 18:119-2, Callet R. Knee Pan and dsablty, 3rd ed. Phladelpha: F.A. Davs, Wojtys EM, Huston LJ. Neuromuscular performance n normal and anteror crucate lgament-defcent lower extremtes. Am J Sports Med 1994; 22: Nelsen S. Knesology of the knee jont. Dan Med Bull 1987;34: Inoue M, McGurk-Burleson E, Holls MJ, Woo SL-Y. Treatment of the medal collateral lgament njury I: The mportance of anteror crucate lgament on varus-valgus knee laxty. Am J Sports Med 1987; 15: Pzal RL, Seerng WP, Nagel DA, Schurman DJ. The functon of the prmary lgaments of the knee n anteror-posteror and medal-lateral motons. J Bomech 198; 13: Toft E, Snkjaer T, Andreassen S, Larsen K. Mechancal and electromyographc responses to stretch of the human ankle extensors. J Neurophysol 1991;65: Pope MH, Johnson RJ, Brown DW, Tghe C. The role of the musculature n njures to the medal collateral lgamen. J Bone Jont Surg (AM) 1979; 61-A: Maquet PGJ. Bomechancs of the knee, 2rd ed. New York: Spnger- Verlag, Inoue M, Woo SL-Y, Gomez MA, Ame D, Ohland KJ, Ktabayash LR. Effects of surgcal treatment and mmoblzaton of the healng of the medal collateral lgament: A long-term multdscplnary study. Connect Tssue Res 199;25: Dllngham MF, Kng WD, Gamburd RS. Rehabltaton of the knee followng anteror crucate lgament and medal collateral lgament njures. Phys Med Rehabl Cln N Am 1994;5:

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