Dor e controle motor

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Dor e controle motor

  1. 1. , II ! ["ITlm HEVfEW The Effect of Musculoskeletal Pain on Motor Activity and Control Michele Sterling, Gwendolen Jull, and Anthony Wright Abstract: Aberrant movement patterns and postures are obvious to elinicians managing patients with musculoskeletal pain. However, some changes in motor function that occur in the presence of pain are less apparent. Clinicai and basic science investigations have provided evidence of the effects of nociception on aspects of motor function. Both increases and decreases in musele activity have been shown, along with alterations in neuronal control mechanisms, proprioception, and local rnusele morpholoqy. Various models have been proposed in an attempt to provide an explanation for some of these changes. These inelude the vicious cyele and pain adaptation models. Recent research has seen the emergence of a new model in which patterns of musele activation and recruitment are altered in the presence of pain (neuromuscular activation model). These changes seem to particularly affect the ability of museles to perform synergistic functions related to maintaining joint stability and control. These changes are believed to persist into the period of chronicity. This review shows current knowledge of the effect of musculoskeletal pain on the motor system and presents the various proposed models, in addition to other shown effects not covered by these models. The relevance of these models to both acute and chronic pain is considered. It is apparent that people experiencing musculoskeletal pain exhibit complex motor responses that may show some variation with the time course of the disorder. © 2001 by the American Pain Society Key words: Musculoskeletal pain, motor function, motor contrai, vicious cycle model, pain adaptation theory, neuramuscular activation model.A berrant movement patterns and postures are obvious spine, cervical spine, and knee.2-4 This 1055 of joint control to and well identified by clinicians managing patients may leave the subject biomechanically vulnerable to further with musculoskeletal pain. injury or be the cause of ongoing pain."Changes in motor activity and contrai observed in the clinic Experimental investigations in both animais and humansinclude increased activity in some muscle graups and have pravided evidence of the eftect of nociception on variousinhibition or weakness of others. In addition, pain avoidance aspects of motor system function. Beth increases andmotor patterns, such as Iimping, decreased ranges of decreases in muscle activity have been shown under certainmovement, listing of the spine, and 1055 of spinal curves, can conditions. From these studies, various models have beenbe observed. Some changes, however, are not 50 apparent. proposed in an attempt to explain motor responses in theMotor control deficits in the form of muscle inhibition and presence of pain. These include the vicious cycle> and painaltered patterns of muscle recruitment, resulting in the loss of adaptation models.f Although these models may go some wayjoint control, recently have been recognized in such areas of toward explaining the effect of pain on motor activity, thethe body as the lumbar scenario that is presented to the clinician, parti cularly in the chronic pain situation, seems to be more complex and highlights the Iimitations of the current models. RecentFrom the Department of Physiotherapy, University of Queensland, Queensland, research supports the emergence of a new model based onAustralia, and the School of Physiotherapy, Curtin University of Technology, Perth,Australia. findings that patterns of muscle activation and recruitment areAddress reprint requests to Professor Anthony Wright, School of Physiotherapy, altered in the presence of paln.?:? Although possibly initiatedCurtin University of Technology, GPO Box U 1987, Perth, WA 6845, Australia.E-mail: twright@curtin.edu.au in the acute stage of injury, these phenomena have been© 2001 by the American Pain Society shown to persist into the period of chronicity.3.4.10•111526-5900101/0203-0007$35.0010doi: 1 0/1 054/jpai.2001.19951 The Journal of Pain, Vai 2, Na 3 (June), 2001: pp 135-145 13 5
  2. 2. 136 Effect of Musculoskeletal Pain on Motor Activity and Control Furthermore, the physiologic mechanisms responsible reflex changes occurred only during the actual period offor pain-evoked motor responses are poorly understood, muscle pain and were not long lastlnq." These findings areparticularly at higher leveis of the central nervous system. suggestive of the involvement of refi ex modulation byAs Chudler and Dong12 observe, little is known about the descending inhibitory activity after intense C fiber input."central mechanisms for integrating incoming nociceptive This is not to say that increased refi ex excitability does notinformation that results in a motor response. It is apparent, occur in human subjects but that ongoing spontaneoushowever, that nociceptive input can have potent effects on pain22 and the involvement of convergent input (spatialthe motor control functions of the central nervous system. summatíon)" may be required for its maintenance.Both peripheral and centrai phenomena have been In addition to nociceptive input from muscle and joints,proposed as explanations of the physiologic changes that nociceptive input from meningeal tissue also producesoccur in the motor system as a result of pain. However, aberrant motor responses. Hu et al 23 showed thatnone of these proposals fully explains the changes application of asma" fiber excitant and inflammatory irritantobserved in the motor system in patients suffering (mustard oil) to meningeal tissues resulted in increasedmusculoskeletal pain. electromyographic (EMG) activity in the neck and jaw The purpose of this review is to show current concepts muscles of rats. They noted especially large EMGand knowledge of the effects of musculoskeletal pain on responses in the trapezius muscle. They suggested thatmotor activity and to present evidence for an emerging the most likely explanation for this increase in EMG activitymodel of altered patterns of neuromuscular control of was central sensitization of trigeminal second ordermuscles that perform key synergistic functions to stabilize nociceptive neurons.the spine and major peripheral joints. Attempts have been made to extrapolate these findings to motor responses observed in specific clinicai syn- dromes. Hall and Quirrtner/" studied 4 subjects with upperIncreased Muscle Activity limb radiculopathy, They showed increased EMG activity inFlexor Withdrawal Reflex the upper trapezius, deltoid, biceps, and triceps muscles After tissue damage, there is a decrease in the threshold after palpation of allodynic nerve tissue in each subject andand an increase in the area of responsiveness and widespread, increased EMG activity in response toduration of response to mechanical stimuli in the norrnally elicitation of myotatic reflexes in the symptomatic upperhighly stable flexor withdrawal reflex.P Strong C fiber input limbs. They suggested that the widespread andfrom skin and particularly from muscle has been shown to multisegmental increase in EMG activity could represent aproduce prolonged sensitization of spinal cord neurons in motor correlate of central sensitization. These changesspinalized rats.!" Intra-articular inflammation produced by could include increased excitability of alpha motor neuronsthe C fiber stimulant mustard Gil also has been shown to and increased excitability of muscle spindles via gamma ,·fproduce a powerful, prolonged facilitation of the flexor motor neurons.?" As described previously, it is believed tiwithdrawal reflex. 1 5, 1 6 that facilitation of alpha motor neurons occurs indirectly via This injury-induced change to the flexor withdrawal refi interneurons in the refi ex pathway," Because theseex seems to depend on central nervous system changes interneurons have divergent connections" their activationrather than sensitization of peripheral afferents.!? In could explain the widespread nature of the EMGinvestigations using intense electrical conditioning responses." Abnormal responses of neurons within thestimulation to a muscle nerve, exaggerated motor dorsal horn (including prolonged afterdischarges to briefresponses were evoked by stimuli applied to distant stimuli and ongoing spontaneous activity) could positivelycutaneous nerves, including those to the opposite limb." influence gamma motor neurons, leading to increasedIn addition, injury-induced changes were not abolished fusimotor drive and sensitization of spindles.>after a sensory block of the injury site with local anesthetic. Increased (possibly protective) rnuscle activity also has17 Because the response properties of both the central been shown in normal subjects when undergoingterminais of the primary afferents and the motor neurons mechanical tests of neurodynamic function (such as thethemselves were normal, it was proposed that the brachial plexus tension test described by El vey26).27 Thesehyperexcitability was due to changes in the interneurons studies support Sunderlands-" proposal that muscle tonethat link the primary afferents with the flexor motor and activity protect the nervous system from tensile forces.neurons.!? It has been suggested that this increase in rnuscle activity Although these effects are long lasting in decerebrate, is due to activation of the flexor withdrawal reflex. 29,3ospinalized preparatlons." in spinally intact animais Although these effects of stimulating nerve tissue havehigh-intensity, repetitive C fiber stimulation results in been shown in normal subjects, Hall et al 31 showed that thedecreased refi ex excitability." Gjerstad et al20 confirmed flexor withdrawal response is more easily elicited inthese findings in human experiments in which inhibition of patients with chronic pain. They investigated hamstringcutaneomuscular reflexes occurred after experimental muscle activity during the straight leg raise test for bothmuscle pain. Andersen et al 21 showed both inhibition and normal subjects and subjects withfacilitation of reflexes, depending on the site of inducedmuscle pain. These
  3. 3. ! > 137 CRITICAL REVIEW/Sterling et ai chronic L5 or S 1 radiculopathy. Their results showed that joints.> rnusde." and skin. 42 If, via this system, afferent hamstring rnusde activity occurred before the onset of pain input has an important effect on motor control, changes in in radiculopathy subjects, whereas in normal subjects, a afferent input due to disease or injury may have important muscle response was only evident after pain was clinicai consequences. However, the precise effect perceived. remains uncertain because of continuing debate as to the These clinicai studies have ali used EMG as a measure nature of the gamma influence, especially with respect to of the rnuscle response to pain. Although EMG activity afferent input from rnuscle, does not necessarily equate to the presence of pain,32 Some studies have suggested an increase in excitability of gamma motor neurons after rnuscle inflammation. increased EMG activity nevertheless does show a Johansson and Sojka5 observed that stimulation of group 111 heightened response of the cutaneomotor reflexes in the and IV rnuscle afferents excites dynamic and static presence of pain. fusimotor neurons, thereby enhancing the sensitivity of Changes in the behavior of spinal cord neurons (centrai primary and secondary muscle spindle afferents that sensitization) after a barrage of nociceptive input are determine rnuscle stiffness. They suggest that increased believed to contribute to the sensory and motor responses activity in primary rnuscle spindle afferents will then increase excitability in alpha motor neurons projecting to the observed clinically.33 It has been proposed that if these primary muscle, They further hypothesize that this central nervous system changes persist, a basis could increased muscle stiffness may lead to increased metabolite exist for the continued presence of clinicai signs (ie, production and further stiffness. In addition, increased increased EMG activity, aberrant movement and postures, activity in the secondary spindle afferents projects back onto and persistent pain) without any ongoing peripheral the gamma system, perpetuating the enhanced rnuscle patholoqy.ê" stiffness. They bel ieve that these effects may be important For central sensitization to be maintained, it is thought in the generation and cause of occupational rnuscle tension (spasm) and pain5.43 and have termed their model the vicious cyc/e that some source of peripheral nociceptive input is mooel. It representsan expansion on a model originally requíred.ê> Suggestions for the source of this input have proposed by Travell et ai in 1942.44 Further studies by included the actions of protective or disused rnusdes or Johanssons group have shown enhanced activity in peripheral scar tlssue.v In addition, it has been suggested primary and secondary spindle afferents after application of that central sensitization can be maintained by chemical mediators such as potassium chloride, lactic acid, subthreshold (initially nonpainful) mechanical stirnuli.ê" bradykinin, and serotonin to rnusde tissue. 43,45,46 In addi- tion to altered responses after local injection into the This would be particularly likely in situations in which the ipsilateral rnusde, these researchers also have shown phenotype of large diameter, myelinated afferent neurons modulation of secondary rnuscle spindle afferents after had changed, allowing them to induce central sensitization injection of bradykinin into the contralateral muscle." in the same manner as unmyelinated C fibers.F Excitatory effects on gamma motor neurons also have Therefore, input produced by sustained or repetitive been shown in the neck rnuscles of the cat. 47 In this study, non-noxious stimuli may maintain central sensitization and increased intramuscular concentration of bradykinin in the be a major source of posthealing pain and an ongoing splenius and trapezius musdes induced large and stimulus for the changes in motor function seen in patients long-Iasting increases in the static stretch-sensitivity of with chronic pain.34 rnuscle spindle afferents from ipsilateral and contralateral rnusdes, thereby lending support to the vicious cycle Modulation of Inhibitory Reflexes hypothesis of Johansson and Sojka. 5 In addition, they Recent studies have shown that pain may have an effect suggested that these findings could contribute to an on inhibitory jaw reflexes. Painful heat stimuli and understanding of the mechanisms behind reduced experimentally induced masseter rnuscle pain have been proprioception and balance and the high frequency of shown to result in modulation of the late suppression dizziness and vertigo in patients with chronic neck pain due periods in human jaw-closing muscles.38-40 These to the interaction between altered proprioceptive input suppression periods are believed to be caused by (from neck muscle spindles) and vestibular íntorrnatíon." inhibitory brain stem modulation elicited by electrical Input from articular afferents also has an effect on stírnulation." Although Wang et aP9 acknowledge that gamma motor neurons.:" He et al,49 in their experiments changes in the inhibitory reflexes were modest and as yet on the response of flexor motor neurons to knee joint the clinicai relevance of this is not clear, it nevertheless inflammation in cats, found both inhibitory and excitatory does provide further information of reflex changes in the effects on gamma motor neurons. Two thirds of the gamma presence of nociception. motor neurons that developed increased refi ex discharges, whereas one third of the neurons supplying the The Vicious Cyc/e Model same rnuscle exhibited reduced refi ex discharges. In addition to increased EMG activity or rnuscle spasm Generation of an inhibitory refi ex response being attributed to effects (albeit indirect) on alpha motor neurons, it has been suggested that excitability in gamma motor neurons may be a cause of increased, rnuscle tension or spasm. ~a_mma or fusimotor neurons are influenced by the discharge of afferents from fi
  4. 4. 138 Effect of Musculoskeletal Pain on Motor Activity and Controlmay balance the influence of excitatory refi ex responses in Although the validity of the vicious cycle model has been some motor neurons, thereby ensuring that the inflamed questioned, there is little doubt that tender, taut musclesjoint is kept in the midrange position where nociceptive joint can be found in patients with musculoskeletal pain. It has afferents are less easily activated as a result of joint been proposed that this may be caused by endogenous inflammation.t" He et ai pointed out that if the hypothesis muscle contracture or alteration in the viscoelastic of cocontraction is correct it would be expected that properties of the muscle (nonelectrical) as opposed to extensor museles should also show a reduced refi ex contractile (electrical) changes. 32 The palpable taut band threshold. However, elinically, the picture is usually one of or trigger point makes the muscle feel tense but is not the development of flexion contractures with joint disease, associated with propagated action potentials that would be slJgge~ting a contraction of flexor muscles and relaxation identified as EMG activity.32 Although this proposal mayof extensor m-uscles.49 They suggested that changes in the sound enticing to both patients and clinicians, the validityrefle-x thresholds of both alpha and gamma motor neurons and reliability of the existence of trigger points have not lead to excitation of flexor motor neurons and result in a been established." flexor refi ex pattern. Following on from this study, Therefore, it would seem that increased muscle activity Johansson and Sjolander43 proposed that afferent may occur in the presence of pain via the flexor withdrawal information from inflamed joints may act to further refi ex (central sensitization) but that ongoing nociceptive increase activity in the gamma musele spindle system, input may be required for it to be sustained. Because the thereby amplifying the vicious cyele model proposed presence of increased resting or postural EMG activity earlier by these investigators. generally has not been shown, heightened flexor However, the vicious cycle model has not been sub- withdrawal responses may only occur with noxious stantiated. Unfortunately, increased EMG activity that provocation such as painful movements. It would seem should be present with increased alpha motor neuron that motor refi ex changes in the presence of pain are activity has not been shown. 51-54 Furthermore, an increase dependent on whether the muscle is at rest or involved in in the refi ex threshold of gamma motor neurons in the static or dynamic activityY Alternatively, painful, taut gastrocnemius group and in the flexor rnusele group muscles palpated at rest in patients with musculoskeletal (tibialis anterior) has been shown after artificially induced syndromes may be caused by changes in the viscoelastic myositis in the gastrocnemius/soleus musele in cats." properties of the muscles themselves and not to the These investigators suggested a reduction in musele tone contractile status of the muscles that could be measured as a possible functional implication of this finding to protect by EMG.32 the damaged tissue. This could be an explanation for the apparent weakness of inflamed museles. It has been speculated that fusimotor inhibition may be the reason for Inhibition or Decrease in Muscle Activity refi ex atrophy of rnuseles in chronic musculoskeletal The Pain Adaptation Model disorders." Lund et al6 refuted the vicious cycle mode!. Theysug- More recently, studies have investigated the influences gested that pain does not cause muscles to become .. of experimental musele pain on spinal reflexes (namely hyperactive but that the ability to contract them is actually the H refi ex and stretch reflexes). The H reflex specifically reduced. The exception to this is when a musele is aCtlng relates to the excitability of alpha motor neurons, whereas as an antagonist, in which case EMG activity has been the stretch reflex also involves musele spindle dynarnícs." shown to be higher than normal in the presence of pain. The short latency stretch reflex has been shown to They argue that this is a useful reflex adaptation that limits increase in both agonist and antagonist muscles" range and velocity of movement, thereby reducing further However, because no H-reflex changes have been found injury and pain. This interaction between muscle pain and after experimental pain, it has been suggested that a muscle coordination has been termed the pain adaptation peripheral mechanism is involved, presumably the delta musele spindle system. 55,56 However, wit~out . evidence modet» Support for the pain adaptation model has been shown by this group in studies involving experimentally of increased excitability of alpha !l.otor _I1eurons, the induced pain in jaw muscles and the zygomatic periosteum vicious cycle model cannot be supportad." Further in both anirnals" and hurnans.> In addition, other investigations have shown that after êxperimentally researchers have shown that maximal voluntary induced muscle pain (in this case, soleus), facilitation of contraction is significantly reduced during saline-induced the stretch refi ex occurs in the relaxed muscle only and muscle pain.53 This has also been shown clinically in not during functional activities such as sitting and walkingY patients with fibromyalgía.60 It is suggested that these However, the effects of pain on stretch reflexes remain changes in motor output originate from alterations in the unresolved beca use no increase in excitability after firing pattern of seg- experimentally induced musele pain in the lumbar spine mental interneurons in the spinal cord or brain stem. 61,62 has been reported." Furthermore, although an increase After saline injection into the gastrocnemius and tibialis has been measured with EMG, an inhibitory effect has anterior muscles, normal subjects showed altered gait been shown in single motor unit recordlnqs.?? coordination due to a decrease of EMG activity in the agonist muscle and an increase in activity in the antagonistic muscle. 53 In addition, saline-induced pain , .-
  5. 5. CRITICAL REVIEW/Sterling et ai 139in the posterior lumbar muscles and pathologic chronic low to other erector spinae muscles (Iongissimus and ilio-back pain result in increased activity in the lumbar costalis). has been detected by using EMG,70 Therefore,paraspinal muscles during periods of the gait cycle in although the net extensor torque remained the same, thewhich, under normal circumstances, these muscles exhibit synergistic influence of lumbar multifidus was dirninished.only minimal activity. Furthermore, reduced EMG activity is Indeed some studies have identified potent changes in theseen in subjects with experimental muscle pain duringperiods of the gait cycle in which these muscles normallyexhibit maximal activity.63 The investigators suggested lumbar multifidus in subjects with low back pain. Hides et al10 used ultrasonography to show a marked atrophy of lumbar multifidus on the side ipsi- f.lateral ,*that these findings correspond with the proposal of Lund et to the patients symptoms and also showed thatal6 that the effect of pain on muscle function is dependent these changes remained even after the patients hadon the action of the muscle, and although it is difficult to ceased to report pain."determine when the back muscles act as agonists or Hodges and Richardson3.7. 8 showed a delay in the onset ofantagonists, it seems that the presence of muscle pain contraction of transversus abdominis in sub- f jects with lowaffects the various phases of the gait cycle in different back pain when they performed limb movements in variousways.53,63 Further support for the pain adaptation model directions. This was in contrast to subjects without low back painhas been produced in studies in which experimental who showed that contraction of transversus abdominis precedesmuscle pain was induced by saline injection into the human the contrac-masseter muscle.64·66 Observed changes included tion of the muscles producing the lirnb movernent. Thesemovements of smaller amplitude, slower movements, and investigators suggested that these findings indi-reduced agonist EMG activity during pain. These motor cate a deficit of motor control, resulting in inefficienteffects may be explained by a facilitatory effect of activity in muscular stabilization of the spine. Transversus abdominisnociceptive muscle afferents on inhibitory brain-stem is thought to provide rotational and lateral con-interneurons during agonist action. 64.67 trol to the spine." This selective activation seems to be Therefore, it would seem that most published evidence lost in individuais who have experienced low back pain.questions the existence of muscle hyperactivity in the OSullivan et al4 reported that subjects with low backpresence of pain, as postulated by the vicious cycle model. pain (in this case spondylolysis or spondylolisthesis)The pain adaptation model has been developed mainly have a different pattern of abdominal muscle activa-from studies involving the induction of experimentai muscle tion when drawing in the abdominal wall muscles in supinepain, which could be argued to be more akin to acute crook Iying compared with pain-free control subjects. Inmuscle pain in the clinicai situation as opposed to chronic this study, subjects with chronic low backpain. Furthermore, this model primarily applies to pain from pain seem to substitute for dysfunction of the deepmuscle and does not really account for pain arising from abdominal muscles by generating greater leveis of activityother tissue such as articular or nerve tissue or pain from in muscles, such as rectus abdominis, to dynamicallyan undetermined source (as occurs in many stabilize the spine. They suggest that this may indicate amusculoskeletal syndromes). This model may have a more dysfunction of neuromuscular control because thelimited application in patients with chronic pain. synergistic function of the deep abdominal muscles is lost and substituted for by rectus abdominis." Cholewicki et al 68 also have suggested that heightened activity in the superficial muscles may be a measurable compensation for loss of segmental spinal support.Altered Patterns of Neuromuscular Activation In the cervical spine, it has been observed that the upper and deep cervical flexor muscles lose their endurance Recently, researchers have begun to investigate pat- capacity in subjects with neck pain and headache_72,73terns of neuromuscular activation. It has been suggested The function of these muscles is considered vital forthat the presence of pain leads to inhibition or delayed cervical segmental stability and postural control_74-76activation of specific muscles or muscle groups that When testing for activity in these muscles, it has beenperform key synergistic functions. This produces noted that patients with neck pain tend to substitute withalterations in the patterns of motor activity and recruitment the superficial flexor muscles (sternocleidomastoid andduring functional movement. It has been suggested that scalenes) to achieve the desired position of the neck.? Inthis inhibition usually occurs in the deep muscles local to addition to these muscles, it also is known that the .the involved joint that perform a synergistic function to .E9J~rior. sub9i.~iEitÇlI "[1lJscl,g,s play an important rolecontrol joint stability.3.4. 7,11,68 with respect to control of the head and neck_75,76 Evidence for altered patterns of neuromuscular control Hallgren et al77 and McPartland et àfl8 noted atrophyinhas been found in various studies. Nouwen_~LaI69 these muscles in patients with chroníc neck pain, It isreported a relative increase in erector spinae activity and a possible that the synergistic function of these muscles isdecrease in lower abdominal activity during lumbar flexion lost and that other muscles,süch as upper trapezius andin subjects with low back pain. Although the pain levator scapulae, substitute for the suboccipital musclesadaptation model may explain these findings, further during functional movements. Upper trapezius and levatorstudies have shown a more complex phenomenono scapulae haveSelective fatigue of lumbar multifidus, as opposed
  6. 6. 140 Effect of Musculoskeletal Pain on Motor Activity and Control been reported to show increased activity in subjects with injury. They suggest that neck proprioception is aftected neck pain.?? by damage to the muscular and articular receptors or by In both the lumbar and cervical spine, it seems that the alteration of afferent integration with respect to headdysfunctional muscles are the deep muscles with élirect orientation in space.P An increase in kinestheticvertebral attachments. These muscles span the vertebrae awareness may be important for pain control. Revel et al90and perform important synergistic supporting functions to showed that improved kinesthesia resulted in a reductionstabilize articular segments rather than being primarily in neck pain in subjects with chronic cervical spine pain.responsible for movement production.80 It seems thatalthough changes in the control of these muscles may beinitiated in the presence of pain and tissue injury, they Pain/Reflex Inhibition oi Musc/eoften are sustained beyond the acute pain phase and may Weakness and wasting of muscles acting around acontribute to the chronicity of many musculoskeletal damaged joint frequently are observed in clinicai practice,problems. The neuromuscular activation model identifies and the phenomenon has been called arthrogenousdysfunction of synergistic muscle control as a specific and musc/e weakness.92 After joint damage, immobilization orimportant consequence of pain and injury. decreased activity due to pain may cause muscle fiber Although most investigations thus far have reported atrophy; however, this cannot explain ali the muscleresults from clinicai studies, some evidence of altered weakness that occurs immediately after injury.92 Therepatterns of motor recruitment has been shown after the also is a reduction in voluntary muscle activation, which isinduction of experimental muscle pain in upper trapez- defined as the failure to fully activate an uninjured muscle,iUS.81 In this study, shoulder muscle coordination was which acts across an injured joint during a maximaladversely influenced and reorganization of the pattern of voluntary contraction.:"muscle recruitment occurred after the induction of This 1055 of maximal contraction may be caused by painexperimental muscle pain in the upper trapezius." inhibition; however, it has been shown that inhibition still occurs when pain is not present.P Painless reflex inhibition is believed to occur when afferent stimuli from a jointNeuronal Control Mechanisms reflexly inhibit the activation of alpha motor neurons in the Apart from local neuromuscular control, other recent ventral horn of the spinal cord. 94 Increased articularresearch has investigated more general neuronal control pressure due to joint effusion has been suggested as amechanisms in patients with musculoskeletal disorders. mechanism for this inhibition. However, aspiration of aByl and Sinnott82 reported that subjects with low back pain joint effusion still does not result in full muscle activation.t"were less likely to be able to balance on 1 foot with their Hurley86 suggested that reduced muscle activation may beeyes closed and showed significantly greater postural caused by abnormal afferent input from damaged jointsway. Venna et al83 observed that subjects with low back structures decreasing the excitability of alpha motorpain and neurologic leg deficits showed significantly neurons. He showed that patients with coexisting anteriorslower reaction times in the upper limbs. Subjects with cruciate ligament ruptures and associated joint damagechronic low back pain also have been shown to have had a greater reduction in quadriceps activation thanslower reaction times (for tasks such as using fingers to patients with isolated anterior cruciate ligament ruptures.push a button in response to light stimuli) than pain-free Most studies on arthrogenous muscle weakness havecontrol subjects, which these investigators suggest could been conducted on knee joints in which quadricepsbe a result of pain. 84 Interestingly, inferior motor and muscle weakness is apparent. However, reduced musclepatient handling skills have been recognized as risk activation is also likely to occur in other areas where jointfactors for back injury in nurses and may be an important damage has occurred. Hides et al 10 showed wasting of thefactor predisposing nurses to spinal pain. 85 lumbar multifidus muscle ipsilateral to the site of symptoms in patients with acute low back pain. McPartland et al78 used magnetic resonance imaging toOther Effects show that subjects with chronic neck pain had marked atrophy of the rectus capitis posterior major and minorProprioceptive Deficits muscles with significant fatty infiltration. Panjabi" sug- Joint damage, which evokes abnormal afferent input gested that any deterioration in muscle function, whichand decreases gamma motor neuron excitability, also may result from disuse, degeneration, disease, or injury,could decrease proprio_ceptiy_e_j!Q,Úty.86 could cause inaccurate feedback to neuronal controlProprioceptive deficits have been shown in peripheral systems, thereby affecting spinal joint control. It couldjoints after traumatic injury,87 chronic degenerative therefore be possible that decreased muscle activationdamage,88 and experimentally induced muscle pain. 89 In caused by either pain or refi ex inhibition may have theaddition to peripheral joints, changes also are evident in potential to affect joint stability. This could have importantthe cervical spine. Revel et al90 found that cervicocephalic implications for ongoing pain and dysfunction.kinesthetic sensibility was significantly poorer in patientswith chronic cervical pain than in normal subjects. Heikkilaand Astrorn" showed a loss of cervicocephalic kinestheticawareness in patients after a whiplash
  7. 7. f .... i· CRITICAL REVIEW/Sterling et ai 141 Muscle Fiber Changes musculoskeletal pain. Some patients may exhibit increased Although this review deals mainly with neuronal control activity in certain muscle groups with simultaneous inhibition mechanisms, it is important to note that local musele changes or decreased activation in others. However, it would seem that occur after tissue injury.96.97 These changes also may none of the mechanisms discussed occurs in isolation and contribute to impaired motor function and control in the therefore does not provide a complete explanation of a presence of pain. patients altered motor function in the presence of pain and It has been suggested that joint injury or immobilization may subsequent to a painful episode. lead to a change in the type or size of muscle fibers. Studies Increased muscle activity certainly is observed elinically but on musclefiber size in the trapezius muscleSof subjects with rarely in isolation, and the vicious cyele model has not been fibromyalgia have shown conflicting results, with some supported by many studies that showed no increase in resting reporting atrophy of type II fibers, whereas others have found EMG activity.41.51.53 Moreover, it has been suggested that no change from control groups.98 there is no elear relation between increased gamma motor Uhlig et al97 investigated muscle fiber changes in ventral neuron drive and muscular hyperactivity albeit in decerebrate (sternocleidomastoid, omohyoid, and longus colli) and dorsal animals.P? (rectus capitis posterior major, obliquus capitis inferior, The pain adaptation model would seem to apply more to splenius capitis, and trapezius) spinal muscles in patients who acute muscle pain in which agonist activity is inhibited and underwent surgery for cervical dysfunction of different antagonistic activity facilitated to protect damaged tissue and etiologies (including rheumatoid arthritis, degenerative prevent further injury. However, the clinicai picture, osteoarthritis, and post-traumatic instability). Signs of muscle particularly in patients with chronic pain, is much more fiber transformations were observed in ali muscles complex than this. Certainly in the acute pain situation, some investigated, as evidenced by an increased rei ative number movements are restricted in this pattern, but other of type IIC fibers. In the ventral muscles and obliquus capitis phenomena also are occurring. In the chronic pain situation, inferior, the occurrence oftransformations correlated with the patients may exhibit a relatively normal range of movement duration of symptoms. In the ventral muscles, the majority of despite the presence of pain and evidence of altered motor transformations were in subjects with symptoms of short control. duration, whereas the obliquus capitis inferior showed fiber Recent research indicates that changes in activation transformations in subjects with long symptom duration. In the patterns of muscles occur in the presence of pain, which other dorsal muscles, no correlation with duration of result in muscles with a synergistic function being inhibited symptoms was found. Because a significantly higher per- and other muscles substituting during functional centage of type IIB fibers were found in muscles that had rnovernent.v? Use of these superficial movement production ceased transformation, these investigators suggest that the muscles as substitutes for the deep local muscles could result transformations occurred in the direction from "slow oxidative" in loss of active joint support and control. Ultimately, this may to "fast glycolytic. "97 lead to ongoing pain or recurrent episodes of pain. There is1 Musele fiber transformations occurred independently of the also some suggestion that changes in motor control systems type of muscle (phasic or tonic), the gender and age of the may occur before the onset of pain and predispose to the patient, the type of condition, and the presence of neurologic development of spinal pain." The neuromuscular activation deficit.97 Because the changes occurred in ali patients model seems to provide an important insight into the chronic irrespective of their condition, the investigators suggested that state in which selective control and activation of specific neck pain itself must be considered the main stimulus for this muscles have been lost. response." It is apparent that subjects suffering musculoskeletal pain These changes in slow twitch muscle fibers could be one have extremely complex motor responses that may show reason for the clinicai observation that the ventral deep neck some variation with the time course of the disorder. flexor muscles show a poor static holding capacity or weakness." Histologic analysis of lumbar multifidus in subjects with lumbar disc herniation also has revealed structural changes. Possible Neurophysiologic Mechanisms Mattila et al96 reported the presence of coretargetoid or "moth-eaten" changes in type I fibers, which they suggested It is c1ear that pain affects and disrupts neuromuscular could be caused by denervation, musele-spasm-induced control. However, the precise neurophysiologic basis for ischemia, or excessive physical strain. Selective atrophy of these changes remains unclear. Few investigators have type 11 musele fibers also has been shown.96.99 hypothesized a mechanism for their findings. Factors such as reflex inhibition due to pain, effusion, or other afferent input may explain some loss of muscular control; however, there may also be supraspinal involvement resulting in loss of balance reactions, postural sway, reduced reaction times, and lhe Clinicai Picture delay in the activation of postural control musc1es associated with limb movements. Each of the phenomena outlined previously can be Brain structures processing afferent information are identified c1inically during assessment of patients with interlinked with those processing motor input in both
  8. 8. 142 Effect of Musculoskeletal Pain on Motor Activity and Control precentral and postcentral gyrus structures.P? In addition, inhibition of others, more subtle anomalous patterns of there is a close anatomic relation between somatosensory neuromuscular activation seem to occur. Some of the models input and motor output in the primary cortices.l" Andersson et discussed (the vicious cycle and pain adaptation rncdels), al,104 using positron emission tomography, showed that .é!!!hough occurring in patients with chronic. pain, clinically brain areas activated by capsaicin-induced peripheral pain seem to bemore applicable in the acute pain situation. Loss of include the anterior cingulate gyrus, the central sulcus, selective activation and inhibition of certain muscles that anterior insular cortex, middle frontal gyrus, and the perform key synergistic functions, leading to altered patterns supplementary motor area. Otte et al,105 also using positron of neuromuscular activation (neuromuscular activation model) emission tomography, showed significant hypometabolism in and the ensuing loss of joint stability and control, are initiated the parieto-occipital cortex in subjects with a whiplash injury, with acute pain and tissue injury. However, these phenomena which they suggested may be caused by activation of persist into the period of chronicity and could be one reason nociceptive afferents from the upper cervical spine. Weiller et for ongoing symptoms. aP03 investigated areas of brain activation during active For optimal treatment, the assessment of patients with movement of the upper limb. These areas included the musculoskeletal pain therefore should include identification of supplementary motor cortex, the inferior parietal córtex, the altered neuromuscular activation as well as assessment of basal ganglia, and the cingulate gyrus. It was apparent that appropriate timing of muscle activation.? patterns of active movement also activated some areas activated by cocontractíon.t" and proprioceptive control.P Exercise nociceptive input. An ongoing barrage of nociceptive input, as programs aimed at training contrai of the deep muscles in the in the chronic pain situation, may potentially affect motor lumbar spine have shown s()_me early success.v! It is output and control. The opposite may also occur, whereby possible that this approach could be applied more widely in active movement (exercise) could potentially modulate the re-education of other muscles that perform synergistic nociception. functions. Little is known about the central nervous system It is also possible that early intervention to reduce the mechanisms responsible for integrating incoming nociceptive barrage of nociceptive input may reduce potential motor information that results in a motor responseY It is possible, control dysfunction. However, some changes in muscle however, that nociceptive input could disrupt central motor function have been shown to occur within 24 hours of injury.l? control mechanisms. Potentially, this could occur at various Therefore, early introduction of exercises aimed at sites within the central nervous system. maintaining motor control patterns may be of considerable importance. It is imperative that further basic research is undertaken to investigate the neurophysiologic mechanisms responsible for Summary and Conclusions these motor changes. At present, the central nervous system mechanisms that integrate nociceptive information into a Musculoskeletal pain potentially produces many motor response are not well defined and require furtherS.!1é;l_ngE;2ill mO!C?Epastivity. Some of these changes can elucidation.be explained by peripheral mechanisms in the musclesthemselves and by mechanisms within the central nervoussystem. Ce;r.tainly, pain has a potent effect on~motor activity aiidcontrÕC . ." - Acknowledgment Thé dysfunction thatõccurs in the neuromuscular system inthe presence of pain is extremely complex. In addition to the This review was prepared with the resources of themore obvious changes, such as increased muscle activity in Department of Physiotherapy, University of Queensland,some muscle groups and Queensland, Australia. References stabilizing exercise in the treatment of chronic low back pain with radiologic diagnosis of spondylolysis ar spondy- 1. Zusman M: Central nervous system contribution to lolisthesis. Spine 22:2959-2967, 1997 mechanically produced motor and sensory responses. Aust J Physiotherapy 38:245-253, 1992 5. Johansson H, Sojka P: Pathophysiological mechanisms 2. 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