2006ISEKCongressKeynoteLectureSensoryMotorcontrolofligamentsandassociatedneuromusculardisordersM.Solomonow*MusculoskeletalDisordersResearchLaboratory,BioengineeringSection,DepartmentofOrthopaedicSurgery,UniversityofColoradoatDenverandHealthSciencesCenter,12800East19thAvenue,Room2103,Mailstop8343,P.O.Box6511,Aurora,Denver,CO80045,USAAbstractThe
ligamentswere considered, overseveral centuries, as themajor
restraints ofthe joints,keeping the associated bonesin
positionandpreventinginstability,e.g.their
separationfromeachotherand/ormal-alignment.Thisproject,conductedover25years,presentsthefollowinghypothesis:1.
Ligamentsarealsomajorsensoryorgans,capableofmonitoringrelevantkinestheticandproprioceptivedata.2.
Excitatoryandinhibitoryreexarcsfromsensoryorganswithintheligamentsrecruit/de-recruitthemusculaturetoparticipateinmaintainingjointstabilityasneededbythemovementtypeperformed.3.
Thesynergyoftheligamentandassociatedmusculatureallocatesprominentroleformusclesinmaintainingjointstability.4.
The viscoelastic properties of ligaments and their classical
responses to static and cyclic loads or movements such as creep,
tensionrelaxation,hysteresisand strainrate
dependencedecreasestheireectivenessasjointrestraintandstabilizersand
assensoryorgansandexposesthejointtoinjury.5. Long-term exposure of
ligaments to static or cyclic loads/movements in a certain
dose-duration paradigms consisting of high loads,long loading
duration, high number of load repetitions, high frequency or rate
of loading and short rest periods develops acute
inam-matoryresponseswhichrequirelongrestperiodstoresolve.Theseinammatoryresponsesareassociatedwithatemporary(acute)neuromusculardisorderandduringsuchperiodhighexposuretoinjuryispresent.6.
Continued exposure of an inamed ligament to static or cyclic load
may result in a chronic inammation and the associated
chronicneuromusculardisorderknownascumulativetraumadisorder(CTD).7.
The knowledge gained from basic and applied research on the sensory
motor function of ligaments can be used as infrastructure
fortranslational research; mostlyforthedevelopmentofsmartorthotic
systemsforligamentdecientpatients.
Threesuchsmartorthosis,forthekneeandlumbarspinearedescribed.8. The
knowledge gained from the basic and applied research manifests in
new physiotherapy modalities for ligament decient
patients.Ligaments, therefore, are important structures with
signicant impact on motor control and a strong inuence on the
quality of
move-ment,safety/stabilityofthejointandpotentialdisordersthatimpactthesafetyandhealthofworkersandathletes.2006ElsevierLtd.Allrightsreserved.1.HistoricalbackgroundFor
centuries the role of the ligaments was thought to bethat of
mechanical structures that maintain the bones asso-ciated with the
joint in a relative position to each other,
e.g.preventtheseparationofthebones. Overtheyearsaddi-tional
informationwas obtainedproviding more detailson the properties of
the ligaments, their anatomy
andmechanicalfunctions.Thecollagenbersoftheligamentswereshowntobeviscoelasticandtheberswereshownto
be at various levels of laxity or tension such that
elonga-1050-6411/$-seefrontmatter
2006ElsevierLtd.Allrightsreserved.doi:10.1016/j.jelekin.2006.08.004*Correspondingauthor.Tel.:+13037240383;fax:+13037240394.E-mailaddress:Moshe.Solomonow@UCHSC.edu.JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxwww.elsevier.com/locate/jelekinARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004tioncreateda
processofrecruitment
whichincreasedwithlengthallowingincreaseintension(WooandBuckwalter,1988;
Woo et al., 1980, 1981, 1987). Furthermore, the posi-tion,
orientation and shape of a specic ligament
wasshowntoalsoincreaseanddecreaseitstensionatspecicrangeof motion,
providingresistancetojoint separationinthat range(Renstromet al.,
1986). It wasalsoshownthat interactionof several ligaments
associatedwiththesamejoint providedjoint stabilityfor most of
therangeofmotioninseveralaxis,allowedequalpressuredistribu-tionof
the twocartilage surfaces andkept the
surfacesmovingonaprescribedtrack.
Suchdataconrmedthemechanicalpropertiesofligamentsasjointstabilizers.Asfarbackastheearly20thcentury,
Payr(1900)sus-pectedthat ligaments mayhave aneurological
functioninadditiontotheirmechanical properties.
Hishypothesiswentwithoutexperimentalprooffornearly50yearsuntilseveral
anatomical studies demonstratedthe existence ofmechanoreceptors in
ligaments (Gardner, 1944; Wrete,1949; FreemanandWyke, 1967a,b;
Ekholmet al., 1960;Patridge,1924).Together with the earlier
demonstration of articularnerves emerging from ligaments (Rudinger,
1857), the pos-sible neurological role of the ligaments as a
sensory elementwasemerging.2.Theligamento-muscularreexAt about the
same time, in the mid-20th century, groupsof Swedish researchers
were attempting to demonstrate thepossibilityof
areexarcfromthekneeligamentstothethighmuscles. Palmer (1938, 1958)
developedtensioninthekneesmedial collateral ligament of
humansandwasabletoseesomemuscleactivityinthesemimembranosus,sartorius,
and vastus muscles and noted decreasing
activityasthetransversetensionviaaligaturewasshifteddistallyalong
the ligament. Stener (1959, 1962) and Andersson andStener(1959),
failedtoobservethereexintheanesthe-tizedfeline, yet
wereabletorecordnerveactivityinthearticularnervesofthefelineandunanaesthetizedhumansuponligamentloading,butnomuscleactivity.Inpatientswithligamentrupture,
painsensationandsomemuscularactivitywas observeduponstretchof
thedamagedliga-ments. It was assumedthat ligament innervationwas
todeliverpainsensationupondamage.The conicting and confusing
results fromthe
twogroupsremaineduntil1987whenwewereabletodemon-strate a distinct
reex activity from the anterior cruciate lig-ament to the
hamstrings in the in vivo feline and
inunanaesthetizedhumansasshowninFig. 1ac(Solomo-now et al., 1987).
Several groups went on to independentlyconrm the existence of a
reex arc fromvariousknee lig-amentstothelegmusclesinhumansandanimal
models(GrabinerandWeiker, 1993; Beardet al., 1994;
Raunestetal.,1996;Sjolander,1989).As the neurological functions of
the knee ligaments andits reexive activationof the thighmuscles
were estab-lished,severalnewquestionsemerged;areallligamentsinthe
major joints innervated and capable of eliciting a reex?Andwhat is
thebiomechanical/physiological
functionofthereexarcfromtheligamentstothemuscles?Overthefollowingyearswehavebeenabletodemon-stratethatmechanoreceptorsexistintheligamentsofthemajor
joints (Guanche et al., 1999; Solomonowet al.,1996;Petrieetal.,
1997,1998)andthatareexarccouldbe elicitedbyeither
electricallystimulatingthe articularnerve emerging fromthe
ligaments or applying tensiondirectlytotheligaments.
Mechanoreceptors andareexarc were demonstrated in the knee, elbow,
shoulder,
ankle,palmarwrist,andlumbarspineasshowninFigs.2and3(Solomonowetal.,
1996, 1998, 2002; Phillipsetal., 1997;Knatt et al., 1995; Guanche
et al., 1995; Stubbs et al.,1998). It is, therefore, a fair
conclusion that most ligamentsare alsoasensoryorganandasource
ofreexarctorele-vantmuscles.Several interestingissues were
alsorevealed. All liga-ments are innervated with the same four
types of aerents;Golgi, Pacinian Corpuscles, Runi endings, and bare
end-ings. Furthermore, insome ligaments these aerents
aredistributed homogenously throughout the length of the lig-ament,
whereasinotherligamentsmostaerentsaredis-tributednear the two
insertions of the ligament tothebone with otherwise poor presences
in their mid-substance.For example, aerents
areevenlydistributedthroughouttheannularandtransversemedial
ligamentsbutneartheinsertions of the radial posterior andanterior
ligamentsoftheelbow(Petrieetal.,1998).Suchndingsgiverisetoseveral
suggestionsregardingtheroleof theligamento-muscularreex.
Onepossibilitysuggeststhat if aerentsaredistributedonlyat
thebonyinsertionoftheligaments,wherethehighertissuestinessresultsinlessstrain,
theexcitationthresholdoftheaer-ents will be elevated and the reex
will become active onlyathighstrains/tensions.
Thismaybeatlevelswhichposea risk for ligament damage and then the
reexivelyrecruited muscular activity may serve to reduce
thestrain/stressintheligament byloadsharing. Conversely,if a
ligament is evenly distributed with aerents, thatmayindicate
anongoingservice as asensoryorganfordetectionofangle, position,
load, joint velocity, etc., e.g.kinesthetic sensing organ. This may
also indicate an ongo-ing synergistic reexive activation of muscles
duringmovement.The absence of Pacinian aerents in the radial
collateralligament of the elbowmayemphasize its role as
ahighthresholdstraindetectororanociceptiverolewherenearinjuriousloadsmaydirectlytriggerareexresponsefromthe
muscles (Petrie et al., 1998), assisting
inpreventinginjury.3.BiomechanicalfunctionsThe biomechanical
functionof the reex initiatedbythe ligaments was proposedbyus tobe
that of ajoint2
M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004stabilizeraswell
asthesourceofco-contractionwhichissonecessaryforrenedandcontrolledmotion.Hirokawaet
al. (1991, 1992)
conductedatwostagestudytoassesstheinteractionofthethighmuscles,quadricepsandham-strings,
andtherelativepositionof thedistal femur andproximal tibia.
Sequential X-rays of cadaver knee weretaken while loading the
quadriceps tendon at dierentloads andthenapplyingloads
tothehamstrings
tendonsimulatingco-contraction,whilethequadricepswerefullyloadedasshowninFig.4.Smallmetalspheresembeddedinthebones,
asintheX-rayof Fig. 5aandb, servedasmarkers that were analyzed
geometrically. The studyshows that anterior translationof the tibia
was elicitedin the range of motion of 60 exion to full extension
withquadriceps loading as shown in Fig. 6a. As the hamstringswere
simultaneouslyloadedas showninFig. 6b, asub-stantial decrease inthe
anterior translationof the tibiaoccurred. It wasclear, therefore,
that thequadricepscanelicit instability andstraininthe ACLdue
toanteriortranslationof theproximal
tibiafrom60exiontofullextension, and that the hamstrings can
substantially
atten-uatetheanteriortranslationwithjustafewpercentofco-activation.We
concluded that reexive activation of the hamstringsas we observed
in the feline and humans (Solomonow et al.,1987)
coulddecreasetheanteriortranslationof
thetibiaanddecreasethetensionintheACL. This isspecicallyapplicable
for the range of motion from 60 degrees exiontonear full extension.
Infull
extensionbothquadricepsandhamstringscouldstienthejointandminimizeinsta-bility,butwithouthavingdirectimpact
onopposingante-rior forces as was shown by Markolf et al. (1976,
1978)
andShoemakerandMarkolf(1982).4.EectsofvelocityandtrainingClearevidencewasprovidedtoexplainthefunctionofthe
ligamento-muscular reex as a synergistic sensory-motor control
scheme for maintaining joint stability,decreasing and/or preventing
risk of damage to theFig. 1. (a) The substantial increase in EMG
activity of the cats hamstring (Trace 1) over 1 s duration (Trace
2) of direct load application (Trace 3) to
theACL.ThequadricepsEMG(Trace4)exhibitsshortinitiallow-levelactivityandthenbecomes
inhibitedforthedurationoftheligamentsloading.(b)Extension torque,
knee angle, hamstring MAV (mean absolute value of the EMG) and EMG,
and quadriceps MAV and EMG obtained from a patientwith a
midsubstance tear of the ACL. Note the large subluxation torque
failure near 42, which appears simultaneously with decrease in
quadriceps EMG/MAV and increase in hamstring EMG/MAV,indicating the
reexive attempt of the muscles to correct the instability.
(c)Extension torque, knee angle,quadricepsMAV, and hamstring MAV
taken fromanACLdecientpatient 2 weekspostarthroscopy.Note that
thetorque doesnotshow any signoffailure, while the reexive decrease
in quadriceps MAV and increase in hamstring MAV do take place near
37 of exion. The patient had abnormally tighthamstrings. Identical
responses were obtained from subjects with hypertrophic knee
muscles due to continuous participation in various exercise and
sportsactivity.M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxx
3ARTICLE IN PRESSPlease cite this article in press as: Solomonow M,
Sensory Motor control of ligaments and associated ..., J.
Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004ligamentviaco-activation.Inaddition,oneoftherolesofongoing
co- activation during various types of joint move-ment was
determinedtobe preserving joint stability
inadditiontoallowingforjointacceleration,dynamicbrak-ingandsmooth,
controlledmotionas showninFig. 7aFig. 2. Typical myoelectric
discharge of the exors digitorum supercialisand profundu, exors
carpi radialis and ulnaris, and the pronator teres inresponse to
stimulation of the median articular nerve to the
medialligamentsoftheelbow.Fig. 3. (a) A typical EMG response of the
four intrinsic foot muscles (FDB, Q, ADM, and AH) to a stimulus
train of 10 pps. (b) A typical EMG
responsetoonepulseshowingthecalculatedtimedelayfromthepeakofthestimulusartifacttothepeakoftheresultingEMG.Fig.
4. Experimental apparatus constructed to x the cadaver knee
whilepermitting loading of the quadriceps and hamstring tendons and
change injointangle.4
M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004and b (Hagood et
al., 1990; Solomonow et al., 1986, 1988,1989; Baratta et al.,
1988). While co-contractionallowsfor a measure of joint stability
throughout normalmotion, the triggering of the ligamento-muscular
reexcanprovideafastdoseofincreaseinjointstabilitywhenunexpectedmovementoccurs,
elicitingsuddenincreaseinligamenttension.Itisaprotectivereex.Wealsodemon-stratedasseeninFig.8,thatinathletes;jumpingactivitycandecrease
the hamstrings coactivationbut that couldbereversedbythreeweeksof
hamstringretraining(Bar-attaet al., 1988).Any protective reex
responding to a potentially damag-ing or risky stimulus must be a
fast-acting one and generateforces in the appropriate muscles.
Review of the studies weconducted on the ligamento-muscular reexes
in the elbow,knee, shoulder, ankle, and spine reveal a response
time (orlatency) ranging from 2.5 to 5 ms (see Fig. 3b for
example).Consideringthelengthofthenervesfromthespinetotherespective
joints, a conduction velocity of 120 ms (for
largeaerentssuchasGolgi andPacinian, Mountcastle, 1974)and a 0.5 ms
for synaptic transmission, only a monosynap-tic or bisynaptic reex
could be assumed. This may empha-size the importance of this reex
as a fast-acting, protectivereex, preventingdamage tothe ligament
andpotentialrisktothejoints.Sofar it was shownthat the ligaments of
the majorjoints and the lumbar spine are equipped with
sensoryorgans; that therearetwopatterns of
thesensoryorgandistributionalongtheligamentwithfunctionalneurologi-cal
implications; that areexarcexistsfromthesensoryreceptors tomuscles
associatedwiththe respective jointandthat thefunctionof
themuscularactivationandco-activation is to unload the ligament
from overload and pre-ventpotentialinjuryordamage.Fig. 5. (a)
Typical radiographof acadaverickneepositionedat 45ofknee exion.
Note the four metal spheres in the femur and the four metalspheres
inthe tibia. (b) Sevensequential quadrangles generatedfromloading
the cadaveric knee (set at 45 of exion) from passive (no load)
upto12 kgloadinthe quadriceps tendon. Note the deformationof
thequadrangleof thepassivestateintheanterior directionas
theloadisincreased,pointingouttheanteriordisplacementofthetibia.F1,F2,T1,andT2correspondtopointsonthefemurandtibia(seeFig.3).Fig.
6. (a) Anteriorposterior displacement of the tibia versus joint
anglefor various load levels in the quadriceps. The horizontal axis
displays thedata of the passive knee (no load). Positive
displacement indicates anteriorshift, while negative displacement
indicates posterior shift. (b) Mean tibiadisplacement versusjoint
angleforconstant 12 kgquadricepsloadandsimultaneous
hamstringsloadsof several magnitudes.
Notedecreaseinanteriortranslationofthetibiaashamstringsloadincreases.M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxx
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Sensory Motor control of ligaments and associated ..., J.
Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.0045.NeuromuscularneutralzonesViscoelastic
tissues, such as ligaments, have classicalresponses to elongation
and tension which includes hyster-esis
andelongationratedependence(Solomonow, 2004).Ligaments can display
large elongations and
relativelylowassociatedtensionwhenstretchedslow.
Fastratesofstretch, however, develop very high tensions that can
resultin severe damage (known as sprain) or rupture at
relativelyshort elongations. Furthermore, when subjected to
astretchandreleasecycle,
thelengthversustensiontrajec-toryduringthestretchisdierentthanthetrajectorydur-ing
the release, e.g. hysteresis. These two mechanicalfactors
areexpectedtohaveasubstantial impact
onthesensory-motorfunctionsoftheligamentsasexpressedbytheligamento-muscularreex.The
above issues were studied and reported in tworeports (Eversull et
al., 2001; Solomonowet al., 2001).We foundthat duringasingle
sinusoidal stretch-releasecycleof thesupraspinous ligament,the
reexwas initiatedonly after a certain length and tension were
developed. Thelengthtensionrangeprior tothetriggeringof thereexwas
properly designated as a neutral zone indicating thatsmall
perturbation (12 mm) in the ligament length aroundits resting
length are probably inconsequential for joint sta-bility and do not
require co-commitant muscular activation(seeFig.9).During the
relaxation phase, the reex disappeared at
adierentlengthanddierentassociatedtension,muchlar-ger than the
length and tension thresholds observed
duringthestretchphaseasseeninFig.9.Duringthestretchphase,
pasttheactivationthresholdof the ligamento-muscular reex, the
EMGgraduallyincreased to the peakand then gradually decreased
duringthe relaxation phase. It was clear that increasing length
andtensionintheligament requiredanincreaseinmuscularforceinorder
tosustainjoint stability. This emphasizedthe synergistic
relationships of ligaments andmuscles
inmaintainingthatstability.FromFig. 9,
onecanalsoseethatasthefrequencyofthesinusoidal
cycleincreasedfrom0.1 Hzto1.0 Hz,
thelengthandtensionthresholdsofthereexdecreased(e.g.reexwastriggeredearlier)duringthestretchphase.Dur-ing
the relaxation phase, the length and tension
thresholdsincreased(e.g.thereexterminatedearlier).Furthermore,as
thestretch-releasecyclefrequencyincreased,
thepeaktopeakEMGanditscorrespondingmeanabsolutevalue(MAV)
increasedas seeninFig. 10, indicatingthat
fastelongationsofligamentsrequiremuchlargercon-commit-tant
muscleforcetomaintainstabilityandminimizethepotential risk of
rupture. For fast ligament
elongation,therefore,higherstinessfromthemusclesprotectthelig-ament
fromdevelopment of hightensionandstrainandpotentialrupture.Fig. 7.
(a) Typical recording of actual trial from one subject at
isokinetic knee velocity of 15 degree/s. Traces show (from top to
bottom) extension andexion normalized torque, knee angle,
normalized quadriceps MAV of its EMG during extension and exion,
and the hamstrings normalized MAV of itsEMG during extension and
exion. Note that the quadriceps MAV during extension and the
hamstrings MAV during exion were nearly constant (despitethe
typical uctuations at maximal force levels) throughout extension
and exion. (b) The antagonist coactivation patterns of the
hamstrings (left column)and quadriceps (right column) are shown for
increasing joint velocity as normalized antagonist EMG (MAV) versus
knee angle. The plots are based on thedata pooled from all
subjects. The vertical bars indicate the standard deviation for
each angle and the curve connects the mean value of the MAV
valuethroughout the range of motion. Note the increase inhamstrings
coactivationwithincreasing velocity just before full
extensionanddecreasingcoactivationattheinitiationofthemotion.6
M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004Finally,
whentheligamentwasexposedtocontinuoussinusoidal stretch-relaxation
cycling, the reex triggerthresholds increased and the termination
thresholdincreasedas well. The peakEMGamplitude decreased.In
essence, prolonged exposure of ligaments to cyclingstretchresults
inlaxityandhysteresis
accompaniedwithsubstantialdecreaseinthedurationandmagnitudeofthereexively
activated muscular forces, exposing the
ligamenttoincreasingpotential riskforinjury.
Thiswastheearlysignthatprolongedcyclingactivityofligamentsisassoci-atedwithriskofinjuryand/oraneuromusculardisorder,whichwillbefullyaddressedlater.6.Ligamentsandtheexion-relaxationphenomenaAssessment
of spinal function, as it relates to the lumbarregion, in
exion-extension requires knowledge and
abilitytodocumenttheexion-relaxationphenomena. Thisphe-nomena
consists of active EMG recorded from the parasp-inal muscles as
anterior exion begins. The EMGamplitude gradually decreases as
exionprogresses
andreachesacompletesilenceatornear4550exion.TheEMGsilencepersiststhroughdeepexionandtheinitialrangeofextension.
Atmid-extensiontheEMGreappearsand increases up to full extension
(Ahern et al., 1988; Allen,1948). Thecurrent understandingisthat
theupperbodymass, whensubjectedtotheeectofgravity, asitmovesinto
exion, requires counter resistance from the
paraspinalmusclestoprevent freecollapseforward. Asexionpro-gresses,
the posterior ligaments (supraspinous, intraspin-ous, posterior
longitudinal, and dorsolumbar fascia)elongateanddeveloptension.
Atsomeangle, inmid-ex-ion, the tension developed in the posterior
ligamentsexceeds therequiredcounter force,
allowingthemusclestorelax.
Furtherexionisassociatedwithcontractionofabdominal muscles
toovercome the increasingforces inFig.10.
Themean(SD)ofthepeakMAVoftheEMGisshownasafunctionoffrequency,
demonstratingthatprogressivelystrongermusclecontractionwasassociatedwithincreasingcyclefrequency.Fig.
8. The average normalized antagonist MAV versus knee angle for
thehamstrings(a)andquadriceps(b)ofnormalsubjectscomparedwiththehamstrings
andquadricepsMAV versuskneeangleofveried athletes (cand d) and
athletes who routinely exercise their hamstrings (e and f).
Theathletes had hypertrophied quadriceps, which resulted in
inhibition of thehamstrings motor drive (EMG) when extension
movement was
performed(seecversusaande).Quadricepcoactivationpatternsofnormalsubjectgroupandathleteswerenearlyidentical.
Thevertical barsateachdatapoint represent the standard deviation
from the mean of all subjects testedinthatcategory.Fig. 9. Typical
hysteresis curves where the tension versus displacement
ofasinglecycleat eachof thefrequenciesemployedisshown;
theperiodwhere the EMG was recorded from its initiation in the
stretch phase to itsterminationinthereleasephaseisdesignated
inboldfaceonthecurve.M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxx
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Electromyogr. Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004the
posterior ligaments. Overall, the process is a
load-shar-ingphenomenabetweenposteriormuscles,
posteriorliga-ments,andabdominalmuscles.Since during exion the
posterior ligaments stretch,
onewouldexpectthatthemechano-receptorswithinthesetis-sues will be
stimulated and trigger paraspinal muscles
con-tractiontoreducetheloadintheligaments. Infact,
theoppositeoccurs; increasedstretchintheligamentsduringdeeper exion
is associated with EMG silence.This imme-diately points out that
perhaps the inhibitory component ofthe ligamento-muscular reex is
active in the
exion-relax-ationprocess.Weconductedaseriesofexperimentstoassesstheroleandfunctionoftheligamento-muscularreexintheex-ion-relaxation
phenomena (Olson et al., 2004, in press,submitted for publication).
In order to oset the
eectofgravity,thesamesubjectgroupwasassesseswhileper-forming
exion-extension from erect posture and from thesupine position
(e.g. sit-ups). The results demonstratedthat inthe sit-upposition,
the exion-relaxationintheparaspinal muscles disappearedandasimilar
patternofactivity (initial EMG activity and silence about the90)
was observedintheabdominal muscles. Thecon-ceptual conclusions
point out the demand for dealing withthe internal moments
(generated by body mass and its ori-entation to the gravity vector)
dictates the pattern of mus-cular activity in strength, timing and
which muscles.
Fromthereexivestandpoint,thisistherstindicationthattheligamento-muscular
reex is substantially modulated
bythespinalandpossiblehighersensoryandmotorneuronsof dierent
systems (proprioceptive, vestibular, etc.) toyieldexcitatoryor
inhibitoryresponses. The mechanicalrequirements to execute the
intended movement, there-fore, are governing the ligamento-muscular
reex responsepattern.Inthelatestreport(Olson et
al.,submittedforpublica-tion),passiveexionextensionwasexecutedwiththeaideof
anactivedynamometer. Thedynamometer supportedthe body mass
throughout the movement.
Surprisingly,muscularactivitywasnotobservedinanyoftheanterioror
posterior muscles. The results support the
assertionmadeintheprevious paragraph, e.g. therewas noneedtosupport
internal orexternal moments(sincethedyna-mometertookcareof all
movements),
andthereexdidnottriggeranymuscularactivity.Atentative,andveryfascinating,conclusionisthattheligamento-muscular
reexis muchmorecomplexthanahard-wired neurological process which
triggers or sup-presses muscles responses uponstretchof
theligaments.The reex is governed by a complex neural network
takingintoaccountjointstability, internal
massanditsimplica-tioninlightof
movementvelocityandacceleration,orien-tationtogravity,etc.Evidently,
much is left to study on the interactions of thevarious components
and internal or external factors
associ-atedwiththeligamento-muscularreex.Itisnotasimplereexbyanystretchoftheimagination.From
the system viewpoint, one can draw the simplieddiagram of Fig. 11
representing the interaction of
ligamentsandthemotorcontrolofajoint.Reconsidering the mechanical
properties of the liga-ments; e.g. creep, tensionrelaxation,
hysteresis, etc. onecan predict from the control diagram of Fig. 11
that severaltypes of neuromuscular disorders
candevelopwithtimewhenperformingoccupationalandsportsactivities.
Simi-larly,aninjuryorruptureofaligamentcouldbeassessedasacauseforaneuromuscularsyndrome.7.ClinicalimplicationsIndeed,
intheearly1980s, alargenumberof
patientswithanteriorcruciateligament(ACL)ruptureunderwentasurgical
repair withasyntheticorautograft frompartof the patellar tendon. In
both cases, the initial results wereencouraging, demonstrating a
measure of restored stabilityintheknee. Overtime, however, it
wasobservedthat theimplanted ligament became lax; that the
quadriceps tendedto atrophy in many patients; that muscular
desynchroniza-tiondue tothe rupture couldbe
restoredwithphysicaltherapy,andthatwithtime,thepatientsdevelopedosteo-arthritic
knees. Overall, conicting and
misunderstoodresponseswereaccumulating, indicatingthat ACLinjuryis
not an isolated decit but most likely a complexsyndrome.With the
help of Fig. 11, one can attempt to gain insightto the logical
chain of events that were observed clinically.1. Rupture of the
ACL, evenif repairedsurgically,
canleaveasensoryperceptive(kinesthetic)decitsincetheaerentsintheligamentsarenotfunctioning(rupturedor
surgically removed). Indeed, Skinner andBarrack(1991)
demonstratedthat patients
withACLrupturedemonstrateddeciencyinkinesthetic perception;
e.g.perceptionofthekneeanglewasdecient. Suchasen-sorydecit
canbeaharbinger of additional damage/injury to the knee when going
up or down stairs, playingsports andperformingoccupational
activities. Indeed,Fig. 11. A control diagram of the forward and
feedback components of
ajointincludingthemuscles,ligaments,andspinalprojections.8
M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004many ACL decient
patients of that time were
reportingwithsecondarykneeinjuryincurredduringdemandingdailyactivity.2.
Quadriceps atrophywas commonlyobservedinACLdecientpatients.
Thenatural responseoforthopaedicsurgeons and physical therapists
was to subject
thepatienttoaquadricepsstrengtheningprogramforsev-eral weeks to
reverse the degeneration. Often, thepatientswiththenowmorepowerful
quadriceps weresubjectedtoadditional
injuryorincreasedepisodesofinstability.A part of the syndrome,
quadriceps muscles at their nor-mal
strengthcangenerateforcesthatincreaseanteriortibial
translationandwiththeabsenceofanACLalsocause ananterior knee
subluxation(Hirokawaet al.,1991, 1992). It seems that while the
ligamento-muscularreexinnormal subjectsexcitesthehamstrings
intherange of motion from 60 exion to full extension, it
alsoinhibits the quadriceps muscles from exerting very largeforces,
preventing subluxation. The concept of
muscularinhibitionattractedlittleattentioninthemotorcontroleld,butitsimplicationsarehighlysignicantforjointstability.
Thequadricepsisapparentlyinhibited, inthenormal subject, from
generating its true maximal forcessuchthat
kneestabilityandoverloadedACLarepre-vented. Inthe ACLdecient
patient the inhibitionissubstantiallylarger
sincethesensoryACLfunctionismissing. Insuchconditions,
evenmoderatequadricepsforce in the range of 65 to full extension
can subluxatethe tibia. The weighted control of the ACL reex
seemstoinhibit the quadriceps as necessaryfor the perfor-mance of
the movement at hand. With its absence, how-ever, deep inhibition
occurs, probably via spinalnetworks. One can conclude that in
addition to theexcitatory reex from ligaments to muscles, there is
alsoaninhibitory ligamento-muscular reex andthat
wasshowninhumansubjectsbyDyhre-PoulsenandKro-gsgaard (2000),
Solomonowand Krogsgaard (2001),Williams andBrance (2004), andVoigt
et al. (1998).The overall objective of the inhibitory and
excitatory
lig-amento-muscularreexistoprovideastableandsafejointmotion.Thequadricepsstrengtheningprogramimplementedinthe
periodprior to1987was acontraindicationas itincreasedtheriskof
sublaxationandthepotential ofnewinjury. Inour report of
1987(Solomonowet al.,1987), we concluded that hamstring
strengthening ismost benecial in the early phase of
ACLdecientpatients rehabilitation, as it will increase the
co-contrac-tionlevel fromthehamstrings,
improvekneestabilityandallowincreasedforceproductionfromthequadri-cepslateron(Solomonowetal.,1989).3.
Muscular balance of the hamstrings and quadriceps,agonistand
itsantagonist,istherefore,oneofthemostimportant aspects in
maintaining knee stability andpreservation of the healthy,
functional ACL. Oneimportant component in balancing an antagonist
musclepairofajointisthesensoryroleofligamentsviatheirinputstothespinal
motorunitsinanexcitatoryand/or inhibitorymode.Indeedseveral groups
managedtodemonstratethatwithanappropriatephysical therapyprogram,
advocating muscle re-education, ACLde-cient patients couldbe
successfully rehabilitatedwithconservative treatment (Giove et al.,
1983; Steineretal.,1986).4. The implications of muscular imbalance
or synchroniza-tion on the gait of patients with ACLdamage
wasrepeatedly reported in the literature (Hasan et al.,1991;
Sinkjaer and Arendt-Nielsen, 1991), and increasedquadriceps
activitywas observedinour researchwithnormal subjects whose ACLwas
statically stretchedanddevelopedcreep(Chuetal., 2003; Sbriccoli
etal.,2005).In such circumstances, the ACL was intact, yet the
laxitydeveloped due to the creep prevented the mechanorecep-tor
within the ligament fromproperly ring at theappropriate threshold
and inhibiting the quadriceps
dur-ingmaximalvoluntaryextension.Itseemsthatruptureof the ACL, for
example, canincrease the inhibitionimposedonamuscle, whereas
stretchedor lax ACLdecreases the inhibition. The exact neural
mechanismof thetwophenomenamayneedfurther study, yet itis clear
that the sensory-motor functions of the
ligamentplaysamajorroleinbothphenomena.8.NeuromusculardisordersassociatedwithligamentsSo
far, neuro-muscular disorders associated with a com-plete ruptureof
a ligament:e.g.desynchronization of ago-nist antagonist activity,
changes in the natural inhibitionof muscles,muscular
atrophy,decientkinesthetic
percep-tionanddecientgaitweredelineated.Inrecentyearsweembarkedontheassessmentofneu-romuscular
disorders associatedwithanintact ligament,yet subjected to
continuous activity such as found in manyoccupational and athletic
environments. Indeed, in
theoccupationaleld,non-speciclowbackdisorders/painisone of the most
common medical problems and is a
costlyproblemfromthestandpointofthelossofwork,medicaltreatment,
andcosttogovernmentandindustry, etc. Thediagnosis and treatment of
such non-specic low back dis-order or as it is also known as
CumulativeTraumaDisor-der (CTD) are poorly developed and/or
understood (NAS,2001).Theepidemiology,however, clearly establishes
therela-tionshipbetweenstaticandrepetitive(cyclic)workactivi-tiesandCTD.
Biomechanical orphysiological validationof the epidemiology is
lacking especially experimentalvalidation.A set of experiments
imposing alternating periods of sta-tic and/or cyclic loadonthe
lumbar supraspinous
liga-mentsyieldedawealthofnewinformation(Claudeetal.,2003;
Courvilleetal., 2005;Gedaliaetal., 1999;
Solomo-M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxx
9ARTICLE IN PRESSPlease cite this article in press as: Solomonow M,
Sensory Motor control of ligaments and associated ..., J.
Electromyogr. Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004now
et al., 1999; Jackson et al., 2001; LaBry et al., 2004; Luet al.,
2004; Navar et al., in press; Sbriccoli et al., 2004a,b,2005, in
press; Solomonow et al., 2003a,b,c; Williams et al.,2000):A.
Substantial creep developed in the ligament within sixperiods of 10
min of load spaced by 10 min of rest. Acontinuous rest periodof
upto78 hafter thesixworkandrestsessionsarenotsucientfortheliga-ment
torecover itsoriginal lengthandstress-straincondition. AsseeninFig.
12, theworkperiodsdis-play gradual decrease of reexive EMG,
spasmsand cumulative creep. The long rest periods is charac-terized
with initial hyperexcitability in muscle activityand very long
recovery of the creep towards thereturnof theligament toits
original restinglengthand normal lengthtension relationship.
Severalimportantissuesshouldbeaddressed: As the creep causes laxity
in the ligament, thethresholdsatwhichtheligamento-muscularreexis
triggered as well as kinesthetic perceptionchange.
Thefeedbacksignal (seeFig. 11), there-fore, is corruptedandresults
infalseperceptionandlowerlevelactivationofthemuscles. False
kinesthetic or proprioceptive perceptionintroduces errors inthe
precisionof movementsandmayresultinanaccidentorinjury.
Thedecreaseinmuscular
activityelicitedbytheligamentousreexalsodecreasesthenormal
sti-nessandstabilityofthelumbarspine,exposingittoincreasingriskofinjury.
Thelongrecoveryperiod(over24 h) requiredtorestore normal ligament
operation renders thelumbar spine to prolonged function with
decreasedprotective capacity and increased exposure
toinjury.Therefore, an acute or transient neuromuscular
disorderexists after a moderate work period during which
anincreased exposure to injury is present due to ligament lax-ity,
reduced muscular activity and false sensory
perception.Theoriginofthisacute/transientdisorderisinthecreep/laxity
oftheligamentanditssensory-motor(neuromuscu-lar) implications
areduetothecorrupt
feedbacksignalsfromthesensoryreceptorswithintheligaments.B. It
wasalsoshownthat several loadingcomponentshave a critical impact on
the development of an acuteinammationintheligament. Decreasingthe
rest periodbetweeneach10 minworksessionfrom10 minto5 min.
Increasingthenumberof repetitions fromsixtoninesessions.
Increasingtheloadfromlowormoderatetohighloadwithinthephysiologicalrange.
Increasing the work/load duration to sustainedperiodsover30
min.Alloftheabovefactorselicitanacuteinammationintheligament(Solomonowetal.,2003a).Theneuromuscu-larcomponentoftheacuteinammationphase,observed23
h aftertheload/rest session is
asignicanthyperexcit-abilityofthemusculaturelastingforseveral
hours. Sinceworkersarerequiredtoreturntheworkthenextday,theFig. 12.
(a) A typical recording of EMG from the L-3/4, L-4/5, and L-5/6
level (top three rows) as well as lumbar displacement and static
load (bottom)recorded from one preparation subjected to a 60-N
load. Note the large-amplitude spasms that are superimposed on the
gradually decreasing EMG duringdierent 10-minute static load
periods. The time axis marked in units of hr. indicates the 7 h
recovery period during which short samples of 12 s loadingwas
appliedtoassess recoveryof creepandEMG. (b)
ThemeanNIEMGdataandthedevelopedmodels for the7
hrecoveryperiodareshownsuperimposedfor20-,40-,and60-Nloads.NotethattheEMGforthe60-Nloadexceedsunity,indicatinghyperexcitabilitydevelopment.10
M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004acuteinammationdoesnothavesucientrestperiodtoheal
the damage (micro-ruptures inthe
collagenbers),thetissueisexposedtoadditionalstretchinganddamage,andwithcontinuedexposure,
developschronicinamma-tion. InFig. 13, samplesof
ligamentswithinammatorysymptoms as evidencedbywidespreadof
neutrophils iscompared to a control sample with few
spontaneousneutrophils. The presence of neutrophils
infusionintheligament was always associated with a
delayedhyperexcitability.Chronic inammation is not a medically
treatableinjury, is degenerative (results inconversionof
ligamentbers tobrous tissue) andis associatedwithpain,
lossofmuscularforce(weakness),reducedrangeofmotionofajointandmusclespasms(Leadbetter,
1990). CTDisanoveruse injury where the ligamentous tissues
becomechronically inamed resulting in permanent
disability(Leadbetter,1990;Solomonowetal.,2003a).Additional
important observations were made. Theworktorest ratioof
1:1wasobservedtobeagoodruleto follow in order to prevent or
attenuate the
developmentofacuteinammation.Thisratio,however,remainedlim-ited to
durations of work and load up to 30 min (e.g.10 minwork: 10
minrest, 20 minwork: 20 minrest, and30 min work: 30 min rest).
Tests at 60 min work and60 min rest resulted in acute inammation.
Long
workperiodscannotbeimplementedwithoutavoidingdamageevenifequaldurationrestisallowed.Fig.13.
(a)Ontherightisaslideshowingthedensityofneutrophilsinaligamentfromthecontrolgroup,notsubjectedtocreep.Onlyspontaneousneutrophilsappear.Ontheleftisaslideshowingtheneutrophil
densityinaligamentsubjectedtooverstimulation.
Thedensityisover4000/mm2asopposed to 36/mm2in the control ligament.
Note the higher magnication on the right slide. (b) A graphical
presentation of the neuromuscular disordersmodel in a case where
the risk factors load, load duration, load to rest ratio and
repetitions were below the risk level. Note that during the
recovery phasethe NIEMG slowly recovers to its normal while the
neutrophil density remains low and steady. (c) A graphical
presentation of the neuromuscular disorderin a case where the risk
factors exceeded the risk threshold triggering a delayed
hyperexcitability associated with acute inammation as expressed by
thesimultaneouslyrisingneutrophildensityintheligaments.Thequestionmarksindicatetimesegmentsforwhichdataiscollectedcurrentlywhereasthecompleteddataisgivenbythenumberofneutrophilspermm2.M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxx
11ARTICLE IN PRESSPlease cite this article in press as: Solomonow
M, Sensory Motor control of ligaments and associated ..., J.
Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004Anacute
neuromuscular disorder associatedwiththecreepof theligament over
timeis thereforepresent andconsists of reduced muscular activity as
work goes on(and decreasedspinal stability), development of
spasmsandthe micro-fracturesin thecollagenbers increase,sig-nicant
increase in muscular activity 67 h after the work iscompleted and
its association with acute inammation.Such an acute neuromuscular
disorder is the rst stepleading tochronic inammation, andthis phase
shouldbe avoidedinany workor sports activity where a fewdays rest
cannot beallowed. Thelong-termimplicationsof inammation and the
associated neuromuscular dis-ability are currently under intense
investigations inourlaboratory.9.ModelofneuromusculardisorderBased
on the large number of experiments on thespinal ligamento-muscular
response to static and cyclicloading(orexion-extension)
wedevelopedamodel thatcanpredict theneuromuscularresponsetoaset of
workand rest sequences. Fromthe model, a determinationcould be made
if a delayed hyperexcitability is
presentandinturnanacuteinammation. Themodel, therefore,canbeuseful
intheassessmentofriskfactors(loadmag-nitude,
loadduration,restduration,loadtorestdurationratioandloadingrepetitions)
ortheirabsenceinagivenwork protocol. Safe work protocols could be
designedalsousingthemodel.The choice of the model was based on the
physiologicaland biomechanical properties of the tissue in
question, e.g.the ligament. It is well established as a
viscoelastic elementwithresponsesaccuratelyestimatedbyexponential
equa-tions. During lumbar exion-extension or knee
exion-extension,theoverallresponseisnotthatofasingleliga-ment but
that of several ligaments, thecartilage, capsuleand in the spine
also the discs and facet capsules. These
dif-ferentcollagentissuesareall viscoelastic, yetthepropor-tion of
viscosity and elasticity is dierent in each one.Thedisc,
forexample, containsgel, auid, initsinternalspace, and therefore is
more viscous than the supraspinousligament or the longitudinal
ligaments. Agood model,therefore,should includebi ortri exponential
componentstodescribetheviscoelasticityofeachofthevariouscolla-gentissuesinordertoprovideaccurateoutput
(Solomo-nowetal.,2000).The original model (Solomonowet al., 2000),
there-fore, includedbi-exponential descriptionof the displace-ment
of thelumbar spineduetostaticor cyclicexion.One component was
utilizedtodescribe the exponentialelongation/deformation due to
brous collagen tissuessuchasligaments, facet capsule,
dorsolumbarfascia, etc.whereas thesecondcomponent was
usedtodescribetheexponential deformationof thelumbar discs
whichcon-tain signicantly more viscosity. The two componentsare
exponential, yet the time constants and coecientsarelargelydierent.
Theconstructedmodel wassuccess-fully used to describe experimental
data with highaccuracy.Furthermore, sincethereexiveEMGwas
elicitedbythedeformationoftheviscoelastictissues,itwasassumedto
follow its deformation pattern; e.g. exponential decrease.That was
executed, also with high accuracy. However, oneissue that
deteriorated the accuracy of the EMG model
wasthespontaneous,unpredictablespasmsthatoccurreddur-ing the
loading periods and also during the followingrecovery. Since the
spasms varied widely in their amplitudeand appeared at any time
duringloading without any pre-dictablepattern, it
isimpossibletomodel thisphenome-non. The spasms
beingsuperimposedonthepredictabledecrease of reexive EMGdue to
viscoelasticdeformationintroduced an unavoidable inaccuracy in the
model,yet allowedthe general patternof the
EMGtoemergefairlyclearly.Therefore, the model developed provides
good estimatesof the deformationof the viscoelastic tissues
duringthedevelopmentof creepand
itsrecoverywithrest.Similarly,thereexivemuscular activitywas
estimatedwell duringthe loading and rest periods. The spasms,
however, shouldbe distinctly noted but lackedrepresentation in the
model.Inour model, we simpliedthe equationinorder toobtainageneral
conceptual behavior of theligamentoneuromuscular responses. Yet,
the accuracy can simplybe optimized if one wishes, just by adding
additional
com-ponentsrepresentingthetissuesathand.Model:Themodelconsideredisbasedonourpreviouswork
where continuous 20-minute static load was followedby a 7-hour
recover period (Solomonow et al., 2000, 2003d;LaBryet al., 2004;
Courville et al., 2005; Claude et al.,2003).TheNormalized
Integrated EMG (NIEMG) during
thecyclicloadingperiodwasdescribedbyEq.(1)asfollows:NIEMGt Aet=T1
NIEMGss1where NIEMGss is the steady state amplitude, A the
ampli-tude of the exponential component, T1 the time constant
oftheexponentialcomponent,andtisthetime.Correspondingly, the
NIEMGduring the
long-termrecoverywasmodeledbythefollowingequationas:NIEMGt
tBet=T2E1 et=T3 Ct TdetTd=T4 NIEMGss2whereB, C,
andEaretheamplitudesofthethreeterms;tBet=T2represents theinitial
hyperexcitability, whichde-cays withinonehour whilereachingits
peakintherst10 min; Ct TdetTd=T4represents the delayed
hyperex-citability; this termis initiated during the rest
period,mostlyafterthesecondhourofrest, withnoeectintherst2 h; E1
et=T3representsthesteadystaterecovery;this term is a slowly rising
exponential throughout the restperiod;
Tdthetimedelayassociatedwiththeinitiationofthedelayedhyperexcitability;
andNIEMGssisthesteadystateamplitudeasdenedinEq.(1).12
M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004InordertoconvertEqs.(1)and(2)todescribeaseriesofworkperiodsspacedbyrestperiods;
twonewcompo-nentsaredened:TWisthetimeperiodoverwhichloadwasappliedtothespine.TRis
the period of rest between any two work periods(TW).n
isthenumberofworkperiods.Eq.(1)describingtheNIEMGbehaviorduringeachoftheworkperiodsisrewrittenasEq.(3):NIEMGt
Anet nTW TRTn1n 1TW TRnTW TR
NIEMGss3It was assumed that Aand NIEMGssare not
constantthroughout thework/rest
periodsandarechangingfromoneworkperiodtothenext.Furthermore,
itwasassumedthatT1mightnotbethesameforalltheworkperiods.Sincethisstudyusesonly10
minofrest,thersttran-sient component of Eq. (2) will be dominant
and the steadystate component contribution as well as the delayed
hyper-excitability term could be neglected for this particular
case.During the rest periods, therefore, the modied Eq. (4) is
asfollow:NIEMGt t n 1TW nTRBnet n 1TW TR
Tn2n 1TW TRn 1TW nTR
NIEMGss4ItwasalsoassumedthattheamplitudesofNIEMGssandBwill
varyfromonerest periodtothenext andthat T2may vary as well. The
graphical representation of themodel after being subject to
non-inammatory andinammatory workloads is shown in Fig. 13b and
c,respectively.Similarly, the equationdescribingthe development
ofdisplacement, a reection of creep of the viscoelastic
tissue,duringaseriesof workperiodsspacedbyrest
periodsisgivenbythefollowingequation:DISPt D0n DLn1 etnTWTRTn5n 1TW
nTRnTW TR
5whereDISP(t) isthedisplacement asafunctionof time,D0n the
elastic component of amplitude,DLn the
viscoelas-ticcomponentofamplitude,
andTn5isthetimeconstantgoverningthedevelopmentofcreepduringexion.The
recovery of the displacement during the rest
periodsisdescribedbythefollowingequation:DISPt D0n Rn DLn
Rnetn1TWnTR
Tn6 n 1TW TRn 1TW nTR
6Such that R is the residual creep at the end of each rest
per-iodandTn6isthe
timeconstantgoverningtherecoveryofcreepineachrestperiod.Again, D0,
DL, andRwereassumedtobeavariablefromonework/restsessiontothenext.
Tn5andTn6werealsoassumedtovaryfromonesessiontothenext.Thelong-termrecoveryafterthework/restsessionwasmodeledbyEq.(2).Once
the mean SDof the experimental data werecalculated, attempts were
made togenerate the best tmodels describedabove
usingtheMarquardtLevenbergnon-linear regression algorithm; in some
cases, thealgorithmfailedtoconvergesatisfactorily;
inthesecases,initial and/or nal values were arrived at by
sequen-tial recursive iteration, optimizing for
regressioncoecient.10.VericationinhumansubjectsTheresearchconductedonCTDdevelopmentwascar-ried
out on the feline. Two distinct projects were conductedusing human
subjects in order to conrm that such neuro-muscular disorders can
be elicited in humans from the sameor similar mechanical inputs
(e.g. high loads, high numberof repetitions, short rest, etc.).
Oneproject examinedtheresponsesofthelumbarparaspinal
musclestoperiodsofstaticandcyclicexion(Solomonowet al., 2003a;
Olsonetal., inpress). Thesecondprojectassessedtheresponseof
theACLof
humansubjectstostaticandcyclicloads(Chuetal.,2003;Sbriccolietal.,2005).Spasms
in the muscles and signicant changes in muscu-lar
synchronizationwas observedafter static andcyclicactivity of the
spine and the knee (see Figs. 14 and 15) con-rmingthedevelopment of
anacutedisorder. Forsafetypurposes, theworkor loadwas
limitedtomildexertionorshortduration,yetitisevidentthatadversefunctionalchangesareelicited.Theresults
inbothprojects
revealthatsimilarresponsetothoseobtainedinthefelineareobservedfromnormal,healthysubjectssubjectedtomildstaticorcyclic(repeti-tive)
activity. Furthermore, similar behavior could
beobtainedfromtheligamentsofthelumbarspineandtheACLoftheknee.Recently,
additional conrmationthatstaticandcycliclumbarexionin humans
elicitsa neuromuscular disordersimilar to thosedepictedin the
felinemodelwere reportedby Granata et al. (2005), Rogers and
Granata (2006), Dic-keyet al. (2003), Kanget al. (2002), McGill
andBrown(1992),andShultzetal.(2004).M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxx
13ARTICLE IN PRESSPlease cite this article in press as: Solomonow
M, Sensory Motor control of ligaments and associated ..., J.
Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.00411.TranslationalresearchclinicalapplicationsAsmostresearch,theultimatebenet
ofmanyyearsofwondering in the dierent highways and alleyways of
basicandappliedmedical investigations is some modicumofpractical
improvement of medical care oered to thepatient population, and the
associated improvement ofthepatientslifestyle.
Preventivemeasuresarealsosigni-cantandbenecial.Thelessonwelearnedsofar
tells us that inorder tomaintain knee stability, weighted
posteriorly directed
forcehastobeappliedtothetibiaintheappropriaterangeofmotion.
Suchaforcecomes
fromtheACLintheintacthumanintherangeofmotionof60exiontonearfullextension.
Furthermore, suchforce is not comingexclu-sively fromthe ACL, but
alsofromthe hamstrings viatheACL-hamstringsreex. IntheACLdecient
patient,theACLtensionis absent andsois thecontributionofthe
hamstrings. In order to allow as close a function to nor-mal as
possible, any external device, e.g. orthosis, needs
tosupplysuchforces.In1983,wesurveyedtheavailablekneebracestoACLdecientpatientsaswellastheliteratureevaluatingthem.It
was clear that most braces consisted of
thigh/calfuprightsandakneejointwithsomeconnectingmembersorstraps.
Aposteriorlydirectedforceintheappropriaterange of motion was not
provided by the braces and the lit-erature evaluating the braces
conrmed that they had
littleimpact,ifany,onkneestabilityasrequired.We developed a new
knee brace (US Patent No.4,781,180) whichincorporatedmechanical
programmablebilateral levers connectedtoananterior retaining
strapplacedovertheproximal tibiaasshowninFig. 16a. Themechanical
programmingwasprovidedbythekneejointsuchthatatnear60exiontheleverswereactivatedanddevelopedaconstant
or
graduallyincreasingposteriorlydirectedforcetotheproximaltibiathroughoutfullexten-sion.
This Smart Brace, therefore, provided the
kneewithasimilarfunctionoftheabsentACL.Initscommercial phase,
theSmartBrace wasavail-able from the Bledsoe Brace System (Grand
Prarie, Texas)and was consequently evaluated by Acierno et al.
(1995). Itwas found, as shown in Fig. 16b, that ACLdecientpatients
could generate isokinetic maximal
voluntaryextensioneortthroughoutthefull
rangeofmotionwithsignicantlyincreasedquadriceps
activationandwithoutFig. 14. (ac) Three typical recordings from
three dierent subjects at 90 and 35 knee angle showing the
extension and exion MVC forces before andafter the10 minloading
session (toptrace), theanterior displacement of thetibia during the
10 min loading period (second tracefrom
top),quadricepsEMG(thirdtrace)andhamstringEMG(bottomtrace).NotethestrongcontinuousburstofspasmsinthequadricepsEMGtraceof(a)fromthe8thminute
to the 11th minute. Similarly, in (b), two bursts of spasms are
seen, one at about the 7th minute and the second just after the
10th minute, with acorresponding spasm in thequadriceps.IN(c) short
bursts of spasms are seen inthe hamstrings EMG throughoutthe 10
minloading period. Note
thelargeincreaseinquadricepsforceatMVC(negativepeak)afterthe10-minuteperiodofloadingtheACL.14
M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004episodes of knee
subluxation. Anoticeable decrease inhamstrings co-activation was
also noted, as it was notrequired. The Smart Brace foundwide
acceptance inclinicsaroundtheworldandperformedwell,especiallyinthe
post-injuryperiodandindaily life of patients withchronicepisodes of
kneesubluxationsecondarytoACLrupture.Oneof thelimitations of
kneebraces madeof metal,plastic or composite materials is that
their weight is appliedtoaninvertedcone, the thigh. During
activity, gravitytendstocausegradualmigrationof thebrace tothe
lowerleg and reduction in its eectiveness. One approach to pre-vent
this problem is the tightening of the attachment strapsto the limb.
This, however, applied excessive pressure to
theskinandoccludedcirculationresultingindiscomfortandpainwithinashortdurationofuse.A
second generation of the Smart Brace, an electronicversion, was
consequently developed and applied (US Pat-ent No. 5,628,722).
Thenewversionconsistedof alightweight elastic sleeve worn over the
knee. A miniature elec-tronic sensor monitored knee angle and
triggered a musclestimulator to deliver weighted activation of the
hamstringsvia surface electrodes incorporated in the elastic
sleeve. Theposteriorly directed force to the proximal tibia
wasdeliveredthis time by the hamstrings which were activatedin the
desired range of motion. The results to dateFig. 15. (ae) Five
typical recordings from ve dierent subjects exposed to cyclic
loading of the ACL for 10 min at 90 and 35. IN the top 2 traces,
theEMG recordings from quadriceps and hamstrings during the
10-minute cycle are shown. The two bottom traces represent the
anterior tibial displacementand the cyclic load, respectively. Note
the presence of EMG spasms in both the quadriceps and hamstrings
(ad). An example with no reex EMG
activityisalsoreported(e).Displ,displacement.M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxx
15ARTICLE IN PRESSPlease cite this article in press as: Solomonow
M, Sensory Motor control of ligaments and associated ..., J.
Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004demonstrate that
the triggeredcoactivationof the ham-strings couldbe adjustedas
necessaryfor the
conditionandconvenienceofthepatientwhilepreventingkneesub-luxation.
An additional nding demonstrated that within afew days of use, a
muscle re-learning occurs, with the spon-taneous hamstrings
coactivation is elevated to prevent sub-luxation even if the Smart
Brace is deactivated (Fig. 17).Similar conditions exist in workers
engaged in repetitive(cyclic) or staticactivities of thelumbar
spine. Theliga-ments and other viscoelastic structures of the
lumbar spinebecomestretchedorlaxafteraperiodofactivityandtheaerents
within the tissues generate a
signicantlydecreasedorcorruptedstimulusforactivationoftheliga-mento-muscularreex.Themuscularactivitywhichmain-tainslumbarstabilitydecreasesorbecomesabsentleavingthespineexposedtoinjury.AlumbarSmartBracewasFig.
16. (a) A schematic of a Smart Brace which generates a function
similar to that of the ACL in the proper range of motion. (b)
Average results fromfour trials for a symptomatic subject showing
average force (top trace), quadricepsMAV, and hamstrings MAV (third
trace) also as a function of
jointangle.NotetheincreaseinquadricepsMAVandthedecreasesinhamstringMAVwhenthebraceisworn,demonstratingareturntonormal
musclefunctionduetotheuseofthebrace.Fig. 17. A schematic diagram of
the electronic version of the Smart ACLBrace where a sensor about
the knee joint triggers surface stimulation
ofthehamstringstopreventexcessiveanteriortranslationofthetibiaandsubluxation.Fig.
18. Aschematic of a lumbar electronic Smart Brace
restoringmuscularforceslostduetocreep/laxityoftheligaments.16
M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004developed (US
Patent No. 5,643,329) (see Fig. 18) and is inthe stage of
evaluation. The brace consists of an elastic gar-ment
commonlywornfordanceorsport withminiaturesensors over the lumbar
spine. A muscle stimulator is acti-vated by the sensors and the
stimulus delivered via
surfaceelectrodesoverthebilateralparaspinalmuscles.Themus-clescontractinaweightedmodeintheappropriaterangeof
motion as we identied in the studies exploring the
ex-ion-relaxation phenomena (Solomonow et al.,
2003a;Olsonetal.,2004,inpress).12.ConclusionsLigaments are not
passive tissue. Fromthe sensorystandpoint andfromtheir
sensory-motor function,
liga-mentsarehighlydynamicandnon-stationary,yetpredict-able
important organs. The inherent structure of
ligamentsandtheirresponsetostaticandcyclicloads, asfoundinwork and
sports activities, allow us to predict non-station-ary behavior as
expressedby creep, hysteresis, tensionrelaxation, etc.
Theseresponsesinturn, diminishactivityof sensory perception and
reexive coordination of muscu-lar activitysuchas
excitationandinhibitionandconse-quentlyreectadverselyonjointstabilityandmovement.The
same stimuli or inputs can adversely aect the liga-ment when
applied for long duration, large loads or repet-itively without
sucient rest to result in an
acuteinammationanditsassociatedacuteneuromusculardis-order.
Theacutedisorderistherststage,
ifnotallowedtoresolvewithsucientrest,ofachronicdisorderwhichis
devastating and non-reversible, inicting misery
andlossestosociety.AcknowledgementsTheauthoracknowledgesthesupport
of theNationalScienceFoundation: GrantsEET8613807,
EET8820772,BCS9207007andBCS9006639. The National Instituteof
Occupational Safety and Health: Grants R01-OH-04079 and
R01-OH-07622. The Occupational
MedicineResearchCenterGrantfromtheLSUBoardofRegents.Theauthoracknowledgesandthanksthemanygraduateandmedical
students, fellows, orthopaedicresidents andassociates who
participated in and contributed to
thislong-termproject.Graduatestudents: S. Acierno(Engineering), L.
Claude(Engineering), A. Courville (Physiology), S. Hagood
(Engi-neering), R. LaBry (Engineering), D. Navar (Neuroscience),M.
Olson (Kinesiology), A. Banks (Engineering), A.
Guzzi(Engineering),S.Hatipkarasulu(Engineering),
R.Baratta(Engineering), H. Hoops (Engineering), N. Patel
(Engineer-ing), P. Le (Engineering), H. Garies (Engineering);
Medicalstudents: C. DAmbrosia, P. DAmbrosia, R. DAmbrosia,D. Chu,
R. LeBlanc, E. Eversull, U. Gedalia, M. Jackson,D. Lu, K. Yousuf,
I. Kopershtein, W. Bose; Orthopaedic res-idents: T. Knatt, J.
Noble, J. Lewis, S. Petrie, J. Collins, D.Phillips, C.
Freudenberger, C. Beck, M. Stubbs, M.
Wil-liams;Fellows:P.Sbriccoli,S.Hirokawa,T.Arabadzhiev;andAssociates:
Professor DAmbrosia(Knee), ProfessorChuinard(Hand),
ProfessorGuanche(Sports), ProfessorWink(Anatomy),
ProfessorLu(Orthopaedics),
ProfessorBaratta(Engineering),ProfessorHarris(Spine),ProfessorDonato(FootandAnkle),
ProfessorZhou(Engineering),Professor Berger (Spine), Professor
Zieske (Pathology), Pro-fessor Gedalia (Rheumatology), Professor Li
(Kinesiology).ReferencesAciernoS, DAmbrosiaC, SolomonowM,
BarattaRV, DAmbrosiaRD. EMGand biomechanics of a dynamic knee brace
for ACLdeciency.Orthopedics1995;18:11017.Ahern M, Follick M,
Council J, et al.. Comparison of
lumbarparavertebraeEMGpatterninchroniclowbackpainpatients
andnon-patients.Pain1988;34:15360.Allen C. Muscle action potentials
used in the study of dynamic
anatomy.BritJPhysMed1948;11:6673.AnderssonS, Stener B. Experimental
evaluationof the hypothesis ofligamento-muscular protective reexes,
II. Astudy in cats usingmedial collateral ligament of the knee
joint. Acta Physiol Scand1959(Suppl.166):2749.Baratta RV, Solomonow
M, Zhou B, Letson D, Chuinard R,
DAmbro-siaR.Muscularco-activation:theroleoftheantagonistmusculatureinmaintainingkneestability.AmJSportMed1988;16:11322.Beard
DJ, Kyberd PJ, OConnor JJ, Fergusson CM, Dodd CAF. Reexhamstring
contraction in anterior cruciate ligament deciency.
JOrthopRes1994;12:21928.Chu D, LeBlanc R, DAmbrosia P, DAmbrosia R,
Baratta RV,Solomonow M. Neuromuscular disorder associated with
anteriorcruciateligamentcreep.ClinBiomech2003;18:22230.ClaudeL,
SolomonowM, ZhouBH, BarattaRV, ZhuM. Neuromus-cular disorder
elicited by cyclic lumbar exion. Muscle
Nerve2003;27:34858.CourvilleA, Sbriccoli P, ZhouBH, SolomonowM,
LuY, Burger E.Short rest periods after static lumbar exionare a
riskfactor
forcumulativelowbackdisorder.JEMGKinesiol2005;15:3752.DickeyJ,
McNortonS, PotvinJ. Repeatedspinal
exionmodulatestheexion-relaxationphenomena.ClinBiomech2003;18:7839.Dyhre-PoulsenP,
KrogsgaardM. Muscularreexeselicitedbyelectricalstimulation of the
anterior cruciate ligament in humans. J Appl
Physiol2000;89:21915.Ekholm J, Eklund G, Skoglung S. On the reex
eects from the knee
jointofthecat.ActaPhysiolScand1960;50:16774.Eversull E, SolomonowM,
ZhouBH, BarattaBV, ZhuM. Neuromus-cular neutral zones sensitivity
to lumbar displacement rate. ClinBiomech2001;16:10213.FreemanM,
WykeB. Theinnervationofthekneejoint:
ananatomicalandhistologicalstudyinthecat.JAnat1967a;101:50532.Freeman
MAR, Wyke B. Articular reexes at the ankle joint:
anelctromyographicstudyofnormalandabnormalinuencesofankle-jointmechanoreceptorsuponreexactivityinthelegmuscles.BritJSurg1967b;54:9901001.Gardner
E. The distribution and termination of nerves in the knee joint
ofthecat.JCompNeurol1944;80:1132.GedaliaU, SolomonowM, ZhouBH,
BarattaRV, LuY, Harris M.Biomechanics of increasedexposure tolumbar
injurydue tocyclicloading: II. Recoveryof
reexivemuscularstabilitywithrest.
Spine1999;24:24617.GioveT,MillerS,KentB.Non-operativetreatmentofthetornACL.JBoneJointSurg1983;G5A:18492.Grabiner
MD, Weiker GC. Anterior cruciate ligament injury
andhamstringscoactivation.ClinBiomech1993;8:2159.GranataK, RogersE,
MoorehouseK.
Eectofstaticexion-relaxationonparaspinalreexbehavior.ClinBiomech2005;20:1624.M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxx
17ARTICLE IN PRESSPlease cite this article in press as: Solomonow
M, Sensory Motor control of ligaments and associated ..., J.
Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004Guanche C,Knatt T,
Solomonow M, Lu Y, Baratta RV.The synergisticaction of the capsule
and shoulder muscles. AmJ Sport Med1995;23:3016.Guanche C, Noble J,
SolomonowM, Wink C. Periarticular
neuralelementsintheshoulder.Orthopedics1999;22:6157.HagoodS,
SolomonowM, BarattaR, ZhouBH, DAmbrosiaR. Theeect of joint
velocityonthecontributionof theantagonist
muscu-laturetokneestinessandlaxity.AmJSportMed1990;18:1827.HasanS,
EdmondstoneM, LimbirdT, Shiavi R, PetersenS.
Reactionforcepatternofinjuredanduninjuredkneesduringwalking.JEMGKinesiol1991;1:21828.HirokawaS,
SolomonowM, LuY, LouZP, DAmbrosiaR. Anteriorposteriorandrotational
displacementofthetibiaelicitedbyquadri-cepscontraction.AmJSportMed1992;20:299306.Hirokawa
S, Solomonow M, Lu Y, Lou ZP, DAmbrosia R. Muscular
co-contractionandcontrol ofkneestability. JEMGKinesiol
1991;1:199208.Jackson M, Solomonow M, Zhou BH, Baratta RV, Harris
M.
MultidusEMGandtensionrelaxationrecoveryafterprolongedstaticlumbarexion.Spine2001;26:71523.KangY,
Choi W, PickarJ. Electrophysiologicevidenceforaninterseg-mental
reex pathway between lumbar paraspinal tissues.
Spine2002;27:E5663.KnattT,Guanche C,Solomonow M,LuY, Baratta
RV,Zhou BH.Theglenohumeral-biceps reex in the feline. Clin Orthop
1995;314:24752.LaBry R, Sbriccoli P, Solomonow M, Zhou BH, Baratta
RV, Lu Y,
ZhuM.Longerstaticexiondurationelicitsaneuromusculardisorderinthelumbarspine.JApplPhysiol2004;96:200515.Leadbetter
W. An introduction to sports-induced soft tissue inammation.In:
Leadbetter W, Buckhalter J, Gordon S, editors. Park Ridge(IL):
AAOS;1990.Lu D, Solomonow M, Zhou BH, Baratta RV, Li L. Frequency
dependentchanges in neuromuscular response to cyclic lumbar exion.
J Biomech2004;37:84555.MarkolfK, Gra-RadfordA, AmstutzH.
Invivokneestability. JBoneJointSurg[Am]1978;60:66474.Markolf K,
Mensch J, Amstutz H. Stiness and laxity of the knee:contributionof
the supportingstructures. J Bone Joint Surg[Am]1976;58:58394.McGill
S, Brown S. Creep response of the lumbar spine to prolonged
fullexion.ClinBiomech1992;17:436.MountcastleV.Medicalphysiology.
St.Louis: C.V.Mosby;1974.Navar D, ZhouBH, LuY, SolomonowM.
Highrepetitionof
cyclicloadingisariskfactorforlumbardisorder.MuscleNerve,inpress.National
Academy of Sciences musculoskeletal disorders and
theworkplace.Washington,DC:NationalAcademyPress;2001.OlsonM, Li L,
SolomonowM. Flexion-relaxationresponse
tocycliclumbarexion.ClinBiomech2004;19:76976.Olson M, Li L,
Solomonow M. Increased passive tissue compliance in thelow back
during passive cycling trunk exion-extension.
Spine,submittedforpublication.Olson M, Solomonow M, Li L.
Flexion-relaxation response to gravity. J.Biomech,inpress.PalmerI.
Ontheinjuriesoftheligamentsofthekneejoints.
ActaChirScand1938(Suppl.53).Palmer I.Pathophysiology of the medial
ligament of the knee joint. ActaChirScand1958;115:3128.Patridge E.
Joints: the limitationof their range of movement
andanexplanationofcertainsurgicalconditions.JAnat1924;58:34654.Payr
E. Der heutige Stand der Gelenkchirugie. Arch Klin
Chir1900;148:40451.Petrie S, Collins J, Solomonow M, Wink C,
Chuinard R, DAmbrosia
R.Mechanoreceptorsinthehumanelbowligaments.JHandSurg[Am]1998;23:5128.Petrie
S, Collins J, Solomonow M, Wink C, Chuinard R. Mechanorecep-tors in
the palmer wrist ligaments. J Bone Joint Surg
1997;79B:4946.Phillips D, Petrie S, Solomonow M, Zhou BH, Guanache
C, DAmbrosiaR. Ligamento-muscularprotectivereexintheelbow.
JHandSurg1997;22A:4738.Raunest J, Sager M, Burgener E.
Proprioceptive mechanisms in thecruciate ligaments: an
electromyographic study on reex activity in thethigh muscles. J
Trauma: Injury, Infection, CritCare 1996;41:48893.RenstromP, Arms
SW, StanwyckTS, JohnsonRJ, PopeMM. Strainwithin the ACL during
hamstring and quadriceps activity. Am J
SportMed1986;14:837.RogersE, GranataK. Disturbedparaspinal
reexfollowingprolongedexion-relaxationandrecovery.Spine2006;31:83945.RudingerN.
DieglenknervendesmenschlichenkroperserlangenVerlagvonFerdinandEnke;1857.Sbriccoli
P, Solomonow M, Zhou BH, Baratta RV, Lu Y, Zhu M, BurgerE. Static
load magnitude is a risk factor in the development
ofcumulativelowbackdisorder.MuscleNerve2004a;29:3008.Sbriccoli P,
SolomonowM, Zhou BH, Lu Y, Work to rest ratiosexceeding unity are a
risk factor for lowback disorder. J
EMGKinesiol,inpress.SbriccoliP,Solomonow M,Zhou BH,Lu Y, Sellards
R. Neuromuscularresponse to cyclic loading of the anterior cruciate
ligament. Am J SportMed2005;33:54351.Sbriccoli P, Yousuf K,
Kopershtein I, Solomonow M, Zhou BH, Zhu M,LuY. Static
loadrepetitionis ariskfactor inthe development oflumbar cumulative
musculoskeletal disorder. Spine
2004b;29:264353.ShoemakerS,MarkolfK.Invivorotarykneestability:ligamentousandmusculaturecontributions.JBoneJointSurg[Am]1982;64:20816.ShultzS,
CarciaC, PerrinD.
Kneejointlaxityaectsmuscleactivationpatterninhealthyknees.JEMGKinesiol2004;14:47583.SinkjaerT,Arendt-NielsenL.KneestabilityandmusclecoordinationinpatientswithACLinjuries.JEMGKinesiol1991;1:20917.Sjolander
P. A sensory role for the cruciate ligaments. Dissertaion,
UmeaUniversity,Umea,Sweden;1989.SkinnerH,Barrack R.Joint position
senseinthe normaland
pathologickneejoint.JEMGKinesiol1991:118090.Solomonow M. Ligaments:
a source of work-related
muculoskeletaldisorder.JEMGKinesiol2004;14:4960.SolomonowM,KrogsgaardM.Sensory-motorcontrolofkneestability.ScandJMedSciSport2001;11:6480.Solomonow
M, Baratta RV, DAmbrosia R. The role of the hamstrings
intherehabilitationoftheACLdecientknee.SportMed1989;7:428.Solomonow
M, Baratta RV, Banks A, Freudenberger C, Zhou B. Flexion-relaxation
response to static lumbar exion. Clin
Biomech2003a;18:2739.Solomonow M, Baratta R, Zhou BH, DAmbrosia R.
EMG coactivationpatterns of the elbow antagonist muscles during
slow isokineticmovement.ExpNeurol1988;100:4707.SolomonowM,
BarattaRV, ZhouBH, BurgerE, ZieskeA, GedaliaA.Muscular dysfunction
elicited by creep of lumbar viscoelastic tissues.
JEMGKinesiol2003b;13:38196.Solomonow M, Baratta R, Zhou BH, Shoji
H, Bose W, Beck C,DAmbrosia R. The synergistic action of the ACL
and thigh muscles
inmaintainingjointstability.AmJSportMed1987;15:20718.Solomonow M,
Eversull E, Zhou B, Baratta RV, Zhu M. Neuromuscularneutral zones
associated with viscoelastic hysteresis during
cycliclumbarexion.Spine2001;26:E31424.Solomonow M, Guzzi A, Baratta
R, Shoji H, DAmbrosia R. EMG-Forcemodel of the elbowantagonist
muscle pair: eect of gravity,
jointpositionandrecruitment.AmJPhysMed1986;65:22342.Solomonow M,
Guanche C, Wink C, Knatt T, Baratta R, Lu Y.Mechanoreceptors and
reex arc in the feline shoulder. J Shoulder
ElbSurg1996;5:13946.SolomonowM, HatipkarasuluS, ZhouBH, BarattaRV,
AghazadehF.Biomechanics and electromyography of a common idiophatic
low backdisorder.Spine2003d;28:123548.SolomonowM, ZhouBH, Baratta
RV, Burger E. Biomechanics andelectromyography of a cumulative
lumbar disorder. Clin Biomech2003c;18:8908.Solomonow M, Zhou BH,
Baratta RV, Lu Y, Harris M. Biomechanics
ofincreasedexposuretolumbarinjuryduetocyclicloading:
Ilossofreexivemuscularstabilization.Spine1999;24:242634.18
M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxxARTICLE
IN PRESSPlease cite this article in press as: Solomonow M, Sensory
Motor control of ligaments and associated ..., J. Electromyogr.
Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004Solomonow M, Zhou
B, Baratta R, Lu Y, Zhu M, Harris M.Biexponential recovery model of
lumbar viscoelastic laxity andreexive muscular activity after
prolonged cyclic loading. ClinBiomech2000;15:16775.SolomonowM,
ZhouBH, BarattaRV, ZhuM, LuY. Neuromusculardisorders associated
with static lumbar exion. J EMGKinesiol2002;12:8190.SolomonowM,
ZhouBH, HarrisM, LuY, BarattaR.
Theligamento-muscularstabilizingsystemofthespine.Spine1998;23:255262.Stener
B. Experimental evaluation of the hypothesis of ligamento-muscular
protective reexes: I. Amethodfor adequate
stimulationofreceptorsinthemedialcollateralligamentofthekneejointofthecat.ActaPhysiolScand1959;48(Suppl.166):526.Stener
B, Petersen I. Electromyographic investigation of reex eects
uponstretching the partially ruptured medial collateral ligament of
the knee.ActaChirScand1962;124:396414.Steiner M, Grana W, Chillag
K. Eect of exercise on the
anteriorposteriorkneelaxity.AmJSportMed1986;14:249.Stubbs M, Harris
M, SolomonowM, ZhouBH, LuY, Baratta RV.Ligamento-muscular
protective reex in the lumbar spine of the
feline.JElectromyogrKinesiol1998;8:197204.US Patent Number
4,781,180, Orthotic Knee Brace System
andMethod.M.SolomonowandR.DAmbrosia;1988.US Patent Number
5,628,722, Method for Maintaining Knee Stability ofaUser Suering
FromDamage ofKneeLigaments.M.SolomonowandR.DAmbrosia;1997.USPatent
Number5,643,329, SystemforMaintainingDesiredSpinalCurvature of a
User Suering FromImproper Alignment of
theVertebraeoftheSpine.M.SolomonowandR.DAmbrosia;1997.VoigtM,
JakabsenJ, SinkjaerT. Non-noxiousstimulusoftheglenohu-meral
jointcapsule elicitsstrong inhibition ofactive
shouldermusclesinconscioushumansubjects.NeuroscienceLetters1998;254:1058.Williams
G, BranceJ. Alteredquadriceps control
inpeoplewithACLdeciency.MedSciSportExer2004;36:108997.Williams M,
Solomonow M, Zhou BH, Baratta RV, Harris M.
Multidusspasmselicitedbyprolongedlumbarexion.Spine2000;25:291624.Woo
SLY, Buckwalter J. Injury and repair of musculoskeletal softtissue.
ParkRidge(IL): AAOS;1988.Woo SLY, Gomez MA, Amiel D, Akeson W. The
eects of exercise on thebiomechanical and biochemical properties of
swine digital
exortendons.JBiomechEng1981;103:516.WooSLY,GomezMA,SitesTJ.Thebiomechanicalandmorphologicalchangesinmedialcollateralligamentoftherabbitaftermobilizationandremobilization.JBoneJoinSurg1987;69A:120011.WooSLY,
Ritter MA, Amiel D, AkesonW. The biomechanical
andbiochemicalpropertiesofswinetendons:
long-termeectsofexerciseonthedigitalextensors.ConnectTissueRes1980;7:17783.Wrete
M. The innervation of the shoulder joint in man. Acta
Anat1949;7:17390.MosheSolomonowPh.D., M.D. (Hon)isaPro-fessor and
director of the Bioengineering Divisionand the Musculoskeletal
Disorders researchLaboratoryintheDepartmentofOrthopedicsatthe
University of Colorado Health SciencesCenter in Denver. He was a
Professor andDirectorof Bioengineeringandof TheOccupa-tional
Medicine Research Center at
LouisianaStateUniversityHealthSciencesCenterinNewOrleans,Louisianafrom1983to2005.He
received the B.Sc. and M.Sc. in ElectricalEngineering
fromCalifornia State University andthe Ph.D. inEngi-neering Systems
and Neuroscience from the University of California,
LosAngeles.Underhisleadership,technologywasdevelopedforseveraltranslationalprojects
related to; Myoelectric control of upper limb prosthetics
foramputees;Electronic walking orthosis for paraplegics; Smart
orthosis forAnterior Cruciate Ligament decient patients; and smart
braces forindividualswithlowbackpain.He is the Founding Editor of
The Journal of Electromyography andKinesiology,
andservesontheEditorial Boardofseveral bioengineeringand medical
journals. Dr. Solomonow is/was a consultant to the
NationalScienceFoundation, National Institutesof Health, Centers
for DiseaseControl, TheVeteransAdministrationandscienticagenciesof
severalEuropean and Asiatic governments and Canada. He was a
councilmemberofthe International Society of Electrophysiological
Kinesiology,the International Societyof Functional Electrical
Stimulation, andtheIEEE-Biomedical EngineeringSociety. He
publishedover 130refereedjournal papers onmusculoskeletal disorders
including: motor control,electromyography, muscle, tendon, ligament
and joint biomechanics,electrical musclestimulation,
prostheticsandorthoticsystemsforpara-plegiclocomotion,
andsupervisedmorethan150engineering, physicaltherapy, medical
students and orthopaedic residents, as well as
post-graduatestudentsandfellowsfromseveralcountries.Dr.
Solomonoworganized the EMGTutorial Workshop in the ISBCongress,
theCanadianSocietyof Biomechanics,
TheHumanFactorsandErgonomicsSociety,andTheSocietyforClinicalMovementAnaly-sis,
wasontheorganizingcommitteeofnumerousconferencesandgavekeynoteandsymposialecturesinmanyothers.
HereceivedtheCrumpAward for Excellence in Bioengineering Research
(UCLA), the DistinctiveContribution Award from Delta 7 Society
(France), The Doctor
MedicineHonorisCausa(VrijeUniversitiet,Brussels),TheI.CahenProfessorship(LSUHSC)andthe1999VolvoAwardforLowBackPainResearch.M.Solomonow/JournalofElectromyographyandKinesiologyxxx(2006)xxxxxx
19ARTICLE IN PRESSPlease cite this article in press as: Solomonow
M, Sensory Motor control of ligaments and associated ..., J.
Electromyogr. Kinesol.(2006),doi:10.1016/j.jelekin.2006.08.004
