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Position Sense in Chronic Pain: Separating Peripheral and Central Mechanisms in Proprioception in Unilateral Limb Pain

  • Anthony J. Tsay
    Correspondence
    Address reprint requests to Mr. Anthony J. Tsay, BBiomed (Hons), School of Psychological Sciences and Monash Institute of Cognitive and Clinical Neurosciences, Building 17, Monash University, Clayton, Victoria 3800, Australia.
    Affiliations
    School of Psychological Sciences and Monash Institute of Cognitive and Clinical Neurosciences, Monash University, Clayton, Victoria, Australia

    Caulfield Pain Management and Research Centre, Caulfield Hospital, Caulfield, Victoria, Australia
    Search for articles by this author
  • Melita J. Giummarra
    Affiliations
    School of Psychological Sciences and Monash Institute of Cognitive and Clinical Neurosciences, Monash University, Clayton, Victoria, Australia

    Caulfield Pain Management and Research Centre, Caulfield Hospital, Caulfield, Victoria, Australia

    School of Public Health and Preventive Medicine, Monash University, Melbourne, Victoria, Australia
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      Highlights

      • Position sense was examined in patients with unilateral chronic pain.
      • A muscular contraction or stretch was used to modulate muscle spindle activity.
      • The unilateral chronic pain groups produced comparable position errors as healthy controls.
      • Painful and nonpainful limbs are involved in limb-matching.
      • Lateralized pain, in the arm or leg, does not influence forearm position sense.

      Abstract

      Awareness of limb position is derived primarily from muscle spindles and higher-order body representations. Although chronic pain appears to be associated with motor and proprioceptive disturbances, it is not clear if this is due to disturbances in position sense, muscle spindle function, or central representations of the body. This study examined position sense errors, as an indicator of spindle function, in participants with unilateral chronic limb pain. The sample included 15 individuals with upper limb pain, 15 with lower limb pain, and 15 sex- and age-matched pain-free control participants. A 2-limb forearm matching task in blindfolded participants, and a single-limb pointer task, with the reference limb hidden from view, was used to assess forearm position sense. Position sense was determined after muscle contraction or stretch, intended to induce a high or low spindle activity in the painful and nonpainful limbs, respectively. Unilateral upper and lower limb chronic pain groups produced position errors comparable with healthy control participants for position matching and pointer tasks. The results indicate that the painful and nonpainful limb are involved in limb-matching. Lateralized pain, whether in the arm or leg, does not influence forearm position sense.

      Perspective

      Painful and nonpainful limbs are involved in bilateral limb-matching. Muscle spindle function appears to be preserved in the presence of chronic pain.

      Key words

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      References

        • Asell M.
        • Sjolander P.
        • Kerschbaumer H.
        • Djupsjobacka M.
        Are lumbar repositioning errors larger among patients with chronic low back pain compared with asymptomatic subjects?.
        Arch Phys Med Rehabil. 2006; 87: 1170-1176
        • Bank P.J.
        • Peper C.E.
        • Marinus J.
        • Beek P.J.
        • Van Hilten J.J.
        Motor dysfunction of complex regional pain syndrome is related to impaired central processing of proprioceptive information.
        J Pain. 2013; 14: 1460-1474
        • Birznieks I.
        • Burton A.R.
        • Macefield V.G.
        The effects of experimental muscle and skin pain on the static stretch sensitivity of human muscle spindles in relaxed leg muscles.
        J Physiol. 2008; 586: 2713-2723
        • Brumagne S.
        • Cordo P.
        • Lysens R.
        • Verschueren S.
        • Swinnen S.
        The role of paraspinal muscle spindles in lumbosacral position sense in individuals with and without low back pain.
        Spine. 2000; 25: 989-994
        • Cleeland C.S.
        • Ryan K.M.
        Pain assessment: Global use of the Brief Pain Inventory.
        Ann Acad Med Singapore. 1994; 23: 129-138
        • Coslett H.B.
        • Medina J.
        • Kliot D.
        • Burkey A.
        Mental motor imagery and chronic pain: The foot laterality task.
        J Int Neuropsychol Soc. 2010; 16: 603-612
        • Cuomo F.
        • Birdzell M.G.
        • Zuckerman J.D.
        The effect of degenerative arthritis and prosthetic arthroplasty on shoulder proprioception.
        J Shoulder Elbow Surg. 2005; 14: 345-348
        • de Oliveira D.C.
        • Barboza S.
        • da Costa F.
        • Cabral M.
        • Silva V.M.
        • Dionisio V.
        Can pain influence the proprioception and the motor behavior in subjects with mild and moderate knee osteoarthritis?.
        BMC Musculoskelet Disord. 2014; 15: 321
        • Descarreaux M.
        • Blouin J.S.
        • Teasdale N.
        Repositioning accuracy and movement parameters in low back pain subjects and healthy control subjects.
        Eur Spine J. 2005; 14: 185-191
        • Fazalbhoy A.
        • Macefield V.G.
        • Birznieks I.
        Tonic muscle pain does not increase fusimotor drive to human leg muscles: Implications for chronic muscle pain.
        Exp Physiol. 2013; 98: 1125-1132
        • Flor H.
        • Braun C.
        • Elbert T.
        • Birbaumer N.
        Extensive reorganization of primary somatosensory cortex in chronic back pain patients.
        Neurosci Lett. 1997; 224: 5-8
        • Flor H.
        • Nikolajsen L.
        • Jensen T.S.
        Phantom limb pain: A case of maladaptive CNS plasticity?.
        Nat Rev Neurosci. 2006; 7: 873-881
        • Gill K.P.
        • Callaghan M.J.
        The measurement of lumbar proprioception in individuals with and without low back pain. Spine.
        (Phila Pa 1976). 1998; 23: 371-377
        • Goble D.J.
        • Lewis C.A.
        • Brown S.H.
        Upper limb asymmetries in the utilization of proprioceptive feedback.
        Exp Brain Res. 2006; 168: 307-311
        • Gregory J.E.
        • Morgan D.L.
        • Proske U.
        Aftereffects in the responses of cat muscle spindles and errors of limb position sense in man.
        J Neurophysiol. 1988; 59: 1220-1230
        • Gregory J.E.
        • Morgan D.L.
        • Proske U.
        Two kinds of resting discharge in cat muscle spindles.
        J Neurophysiol. 1991; 66: 602-612
        • Guerraz M.
        • Provost S.
        • Narison R.
        • Brugnon A.
        • Virolle S.
        • Bresciani J.P.
        Integration of visual and proprioceptive afferents in kinesthesia.
        Neuroscience. 2012; 223: 258-268
        • Ha S.M.
        • Kwon O.Y.
        • Yi C.H.
        • Jeon H.S.
        • Lee W.H.
        Effects of passive correction of scapular position on pain, proprioception, and range of motion in neck-pain patients with bilateral scapular downward-rotation syndrome.
        Man Ther. 2011; 16: 585-589
        • Haggard P.
        • Iannetti G.D.
        • Longo M.R.
        Spatial sensory organization and body representation in pain perception.
        Curr Biol. 2013; 23: R164-R176
        • Harvie D.S.
        • Broecker M.
        • Smith R.T.
        • Meulders A.
        • Madden V.J.
        • Moseley G.L.
        Bogus visual feedback alters onset of movement-evoked pain in people with neck pain.
        Psychol Sci. 2015; 26: 385-392
        • Hodges P.W.
        Changes in motor planning of feedforward postural responses of the trunk muscles in low back pain.
        Exp Brain Res. 2001; 141: 261-266
        • Hodges P.W.
        • Tucker K.
        Moving differently in pain: A new theory to explain the adaptation to pain.
        Pain. 2011; 152: S90-S98
        • Holmes N.P.
        • Spence C.
        Visual bias of unseen hand position with a mirror: spatial and temporal factors.
        Exp Brain Res. 2005; 166: 489-497
        • Izumizaki M.
        • Tsuge M.
        • Akai L.
        • Proske U.
        • Homma I.
        The illusion of changed position and movement from vibrating one arm is altered by vision or movement of the other arm.
        J Physiol. 2010; 588: 2789-2800
        • Johansson H.
        • Sojka P.
        Pathophysiological mechanisms involved in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes: A hypothesis.
        Med Hypotheses. 1991; 35: 196-203
        • Knox J.J.
        • Beilstein D.J.
        • Charles S.D.
        • Aarseth G.A.
        • Rayar S.
        • Treleaven J.
        • Hodges P.W.
        Changes in head and neck position have a greater effect on elbow joint position sense in people with whiplash-associated disorders.
        Clin J Pain. 2006; 22: 512-518
        • Lackner J.R.
        • Taublieb A.B.
        Influence of vision on vibration-induced illusions of limb movement.
        Exp Neurol. 1984; 85: 97-106
        • Lam S.S.
        • Jull G.
        • Treleaven J.
        Lumbar spine kinesthesia in patients with low back pain.
        J Orthop Sports Phys Ther. 1999; 29: 294-299
        • Lee A.S.
        • Cholewicki J.
        • Reeves N.P.
        • Zazulak B.T.
        • Mysliwiec L.W.
        Comparison of trunk proprioception between patients with low back pain and healthy controls.
        Arch Phys Med Rehabil. 2010; 91: 1327-1331
        • Lefaucheur J.P.
        • Drouot X.
        • Ménard-Lefaucheur I.
        • Keravel Y.
        • Nguyen J.P.
        Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain.
        Neurology. 2006; 67: 1568-1574
        • Lewis J.S.
        • Kersten P.
        • McPherson K.M.
        • Taylor G.J.
        • Harris N.
        • McCabe C.S.
        • Blake D.R.
        Wherever is my arm? Impaired upper limb position accuracy in complex regional pain syndrome.
        Pain. 2010; 149: 463-469
        • Longo M.R.
        Implicit and explicit body representations.
        Eur Psychol. 2015; 20: 6-15
        • Longo M.R.
        • Haggard P.
        An implicit body representation underlying human position sense.
        Proc Natl Acad Sci U S A. 2010; 107: 11727-11732
        • Lotze M.
        • Moseley G.L.
        Role of distorted body image in pain.
        Curr Rheumatol Rep. 2007; 9: 488-496
        • Lovibond P.F.
        • Lovibond S.H.
        The structure of negative emotional states: Comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories.
        Behav Res Ther. 1995; 33: 335-343
        • May A.
        Chronic pain may change the structure of the brain.
        Pain. 2008; 137: 7-15
        • Miller R.P.
        • Kori S.
        • Todd D.
        The Tampa Scale: A measure of kinesiophobia.
        Clin J Pain. 1991; 7: 51-52
        • Morgan D.L.
        • Prochazka A.
        • Proske U.
        The after-effects of stretch and fusimotor stimulation on the responses of primary endings of cat muscle spindles.
        J Physiol. 1984; 356: 465-477
        • Mörl F.
        • Matkey A.
        • Bretschneider S.
        • Bernsdorf A.
        • Bradl I.
        Pain relief due to physiotherapy doesn’t change the motor function of the shoulder.
        J Bodyw Mov Ther. 2011; 15: 309-318
        • Moseley G.L.
        • Flor H.
        Targeting cortical representations in the treatment of chronic pain: A review.
        Neurorehabil Neural Repair. 2012; 26: 646-652
        • Moseley G.L.
        • Gallace A.
        • Di Pietro F.
        • Spence C.
        • Iannetti G.D.
        Limb-specific autonomic dysfunction in complex regional pain syndrome modulated by wearing prism glasses.
        Pain. 2013; 154: 2463-2468
        • Moseley G.L.
        • Gallace A.
        • Iannetti G.D.
        Spatially defined modulation of skin temperature and hand ownership of both hands in patients with unilateral complex regional pain syndrome.
        Brain. 2012; 135: 3676-3686
        • Moseley G.L.
        • Gallace A.
        • Spence C.
        Space-based, but not arm-based, shift in tactile processing in complex regional pain syndrome and its relationship to cooling of the affected limb.
        Brain. 2009; 132: 3142-3151
        • Newcomer K.
        • Laskowski E.R.
        • Yu B.
        • Larson D.R.
        • An K.N.
        Repositioning error in low back pain: Comparing trunk repositioning error in subjects with chronic low back pain and control subjects.
        Spine. 2000; 25: 245-250
        • Newcomer K.L.
        • Laskowski E.R.
        • Yu B.
        • Johnson J.C.
        • An K.N.
        Differences in repositioning error among patients with low back pain compared with control subjects.
        Spine. 2000; 25: 2488-2493
        • O’Sullivan P.B.
        • Burnett A.
        • Floyd A.N.
        • Gadsdon K.
        • Logiudice J.
        • Miller D.
        • Quirke H.
        Lumbar repositioning deficit in a specific low back pain population.
        Spine. 2003; 28: 1074-1079
        • Parsons L.M.
        Imagined spatial transformations of one’s hands and feet.
        Cogn Psychol. 1987; 19: 178-241
        • Parsons L.M.
        Integrating cognitive psychology, neurology and neuroimaging.
        Acta Psychol. 2001; 107: 155-181
        • Paulus I.
        • Brumagne S.
        Altered interpretation of neck proprioceptive signals in persons with subclinical recurrent neck pain.
        J Rehabil Med. 2008; 40: 426-432
        • Pötzl W.
        • Thorwesten L.
        • Götze C.
        • Garmann S.
        • Steinbeck J.
        Proprioception of the shoulder joint after surgical repair for instability: A long-term follow-up study.
        Am J Sports Med. 2004; 32: 425-430
        • Proske U.
        The role of muscle proprioceptors in human limb position sense: A hypothesis.
        J Anat. 2015; 227: 178-183
        • Proske U.
        • Gandevia S.C.
        The proprioceptive senses: Their roles in signaling body shape, body position and movement, and muscle force.
        Physiol Rev. 2012; 92: 1651-1697
        • Proske U.
        • Morgan D.L.
        • Gregory J.E.
        Thixotropy in skeletal muscle and in muscle spindles: A review.
        Prog Neurobiol. 1993; 41: 705-721
        • Proske U.
        • Tsay A.
        • Allen T.
        Muscle thixotropy as a tool in the study of proprioception.
        Exp Brain Res. 2014; 232: 3397-3412
        • Schwoebel J.
        • Friedman R.
        • Duda N.
        • Coslett H.B.
        Pain and the body schema. Evidence for peripheral effects on mental representations of movement.
        Brain. 2001; 124: 2098-2104
        • Sheeran L.
        • Sparkes V.
        • Caterson B.
        • Busse-Morris M.
        • van Deursen R.
        Spinal position sense and trunk muscle activity during sitting and standing in nonspecific chronic low back pain: Classification analysis.
        Spine. 2012; 37: E486-E495
        • Stanton T.R.
        • Lin C.W.
        • Bray H.
        • Smeets R.J.
        • Taylor D.
        • Law R.Y.
        • Moseley G.L.
        Tactile acuity is disrupted in osteoarthritis but is unrelated to disruptions in motor imagery performance.
        Rheumatology (Oxford). 2013; 52: 1509-1519
        • Tsay A.
        • Allen T.J.
        • Proske U.
        Position sense at the human forearm after conditioning elbow muscles with isometric contractions.
        Exp Brain Res. 2015; 233: 2635-2643
        • Tsay A.
        • Allen T.J.
        • Proske U.
        • Giummarra M.J.
        Sensing the body in chronic pain: A review of psychophysical studies implicating altered body representation.
        Neurosci Biobehav Rev. 2015; 52: 221-232
        • Tsay A.
        • Giummarra M.
        • Allen T.J.
        • Proske U.
        The sensory origins of human position sense.
        J Physiol. 2016; 594: 1037-1049
        • Tsay A.
        • Savage G.
        • Allen T.J.
        • Proske U.
        Limb position sense, proprioceptive drift and muscle thixotropy at the human elbow joint.
        J Physiol. 2014; 592: 2679-2694
        • Turton A.J.
        • Palmer M.
        • Grieve S.
        • Moss T.P.
        • Lewis J.
        • McCabe C.S.
        Evaluation of a prototype tool for communicating body perception disturbances in complex regional pain syndrome.
        Front Hum Neurosci. 2013; 7: 517
        • White O.
        • Proske U.
        Illusions of forearm displacement during vibration of elbow muscles in humans.
        Exp Brain Res. 2009; 192: 113-120