Skip to main content

Central Nervous System Adaptation After Ligamentous Injury: a Summary of Theories, Evidence, and Clinical Interpretation

Abstract

The array of dysfunction occurring after ligamentous injury is tied to long-term clinical impairments in functional performance, joint stability, and health-related quality of life. To appropriately treat individuals, and in an attempt to avoid sequelae such as post-traumatic osteoarthritis, investigators have sought to better establish the etiology of the persistent dysfunction present in patients who have sustained joint ligament injuries to the lower extremities. Recent evidence has suggested that changes within the brain and central nervous system may underlie these functional deficits, with support arising from direct neurophysiologic measures of somatosensory dysfunction, motor system excitability, and plasticity of neural networks. As research begins to utilize these findings to develop targeted interventions to enhance patient outcomes, it is crucial for sports medicine professionals to understand the current body of evidence related to neuroplasticity after ligamentous injury. Therefore, this review provides (1) a comprehensive and succinct overview of the neurophysiologic techniques utilized in assessing central nervous system function after ligamentous injury, (2) a summary of the findings of previous investigations utilizing these techniques, and (3) direction for further application of these techniques in the prevention and rehabilitation of joint injury.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. 1.

    Nunez M, Sastre S, Nunez E, et al. Health-related quality of life and direct costs in patients with anterior cruciate ligament injury: single-bundle versus double-bundle reconstruction in a low-demand cohort—a randomized trial with 2 years of follow-up. Arthroscopy. 2012;28(7):929–35.

    PubMed  Article  Google Scholar 

  2. 2.

    Mather RC 3rd, Koenig L, Kocher MS, et al. Societal and economic impact of anterior cruciate ligament tears. J Bone Joint Surg Am. 2013;95(19):1751–9.

    PubMed  PubMed Central  Article  Google Scholar 

  3. 3.

    De Boer AS, Schepers T, Panneman MJ, et al. Health care consumption and costs due to foot and ankle injuries in the Netherlands, 1986–2010. BMC Musculoskelet Disord. 2014;15:128.

    PubMed  PubMed Central  Article  Google Scholar 

  4. 4.

    Freeman MA. Instability of the foot after injuries to the lateral ligament of the ankle. J Bone Joint Surg Br. 1965;47(4):669–77.

    CAS  PubMed  Google Scholar 

  5. 5.

    McCluskey G, Blackburn TA. Classification of knee ligament instabilities. Phys Ther. 1980;60(12):1575–7.

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Oiestad BE, Engebretsen L, Storheim K, et al. Knee osteoarthritis after anterior cruciate ligament injury: a systematic review. Am J Sports Med. 2009;37(7):1434–43.

    PubMed  Article  Google Scholar 

  7. 7.

    Valderrabano V, Hintermann B, Horisberger M, et al. Ligamentous posttraumatic ankle osteoarthritis. Am J Sports Med. 2006;34(4):612–20.

    PubMed  Article  Google Scholar 

  8. 8.

    Needle AR, Swanik CB, Schubert M, et al. Decoupling of laxity and cortical activation in functionally unstable ankles during joint loading. Eur J Appl Physiol. 2014;114(10):2129–38.

    PubMed  Article  Google Scholar 

  9. 9.

    Pietrosimone BG, McLeod MM, Lepley AS. A theoretical framework for understanding neuromuscular response to lower extremity joint injury. Sports Health. 2012;4(1):31–5.

    PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Lepley AS, Strouse AM, Ericksen HM, et al. Relationship between gluteal muscle strength, corticospinal excitability, and jump-landing biomechanics in healthy women. J Sport Rehabil. 2013;22(4):239–47.

    PubMed  Article  Google Scholar 

  11. 11.

    Hopkins J, Ingersoll CD. Arthrogenic muscle inhibition: a limiting factor in joint rehabilitation. J Sport Rehabil. 2000;9(2):135–59.

    Article  Google Scholar 

  12. 12.

    Swanik CB. Brains and sprains: The brain’s role in noncontact anterior cruciate ligament injuries. J Athl Train. 2015;50(10):1100–2.

    PubMed  Article  Google Scholar 

  13. 13.

    Ericksen HM, Lepley AS, Gribble PA, et al. Cortical excitability of the quadriceps is decreased in individuals with unilateral anterior cruciate ligament reconstruction. J Athl Train. 2011;46(3):S-36.

  14. 14.

    Pietrosimone BG, McLeod MM, Ko JP, et al. Chronic ankle instability and corticomotor excitability of the fibularis longus muscle. J Athl Train. 2012;47(6):621–6.

    PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Kapreli E, Athanasopoulos S, Gliatis J, et al. Anterior cruciate ligament deficiency causes brain plasticity: a functional MRI study. Am J Sports Med. 2009;37(12):2419–26.

    PubMed  Article  Google Scholar 

  16. 16.

    Wikstrom EA, Hubbard-Turner T, McKeon PO. Understanding and treating lateral ankle sprains and their consequences: a constraints-based approach. Sports Med. 2013;43(6):385–93.

    PubMed  Article  Google Scholar 

  17. 17.

    Needle AR, Charles BBS, Farquhar WB, et al. Muscle spindle traffic in functionally unstable ankles during ligamentous stress. J Athl Train. 2013;48(2):192–202.

  18. 18.

    Rosen A, Swanik C, Thomas S, et al. Differences in lateral drop jumps from an unknown height among individuals with functional ankle instability. J Athl Train. 2013;48(6):773–81.

  19. 19.

    Houck JR, De Haven KE, Maloney M. Influence of anticipation on movement patterns in subjects with ACL deficiency classified as noncopers. J Orthop Sports Phys Ther. 2007;37(2):56–64.

    PubMed  Article  Google Scholar 

  20. 20.

    Houck JR, Wilding GE, Gupta R, et al. Analysis of EMG patterns of control subjects and subjects with ACL deficiency during an unanticipated walking cut task. Gait Posture. 2007;25(4):628–38.

    PubMed  Article  Google Scholar 

  21. 21.

    Munn J, Sullivan SJ, Schneiders AG. Evidence of sensorimotor deficits in functional ankle instability: a systematic review with meta-analysis. J Sci Med Sport. 2010;13(1):2–12.

    PubMed  Article  Google Scholar 

  22. 22.

    Gokeler A, Benjaminse A, Hewett TE, et al. Proprioceptive deficits after ACL injury: are they clinically relevant? Br J Sports Med. 2012;46(3):182–92.

    Article  Google Scholar 

  23. 23.

    Konradsen L. Sensori-motor control of the uninjured and injured human ankle. J Electromyogr Kinesiol. 2002;12(3):199–203.

    CAS  PubMed  Article  Google Scholar 

  24. 24.

    Chinn L, Dicharry J, Hertel J. Ankle kinematics of individuals with chronic ankle instability while walking and jogging on a treadmill in shoes. Phys Ther Sport. 2013;14(4):232–9.

    PubMed  Article  Google Scholar 

  25. 25.

    Gutierrez GM, Knight CA, Swanik CB, et al. Examining neuromuscular control during landings on a supinating platform in persons with and without ankle instability. Am J Sports Med. 2012;40:193–201.

    PubMed  Article  Google Scholar 

  26. 26.

    Valeriani M, Restuccia D, Di Lazzaro V, et al. Central nervous system modifications in patients with lesion of the anterior cruciate ligament of the knee. Brain. 1996;119(Pt 5):1751–62.

    PubMed  Article  Google Scholar 

  27. 27.

    Baumeister J. Sensorimotor control and associated brain activity in sports medicine research. Paderborn: Universitat Paderborn; 2013.

    Google Scholar 

  28. 28.

    Cohen LG, Starr A, Pratt H. Cerebral somatosensory potentials evoked by muscle stretch, cutaneous taps and electrical stimulation of peripheral nerves in the lower limbs in man. Brain. 1985;108(1):103–21.

    CAS  PubMed  Article  Google Scholar 

  29. 29.

    Sur S, Sinha VK. Event-related potential: an overview. Ind Psychiatry J. 2009;18(1):70–3.

    PubMed  PubMed Central  Article  Google Scholar 

  30. 30.

    Huang CY, Hwang IS. Behavioral data and neural correlates for postural prioritization and flexible resource allocation in concurrent postural and motor tasks. Hum Brain Mapp. 2013;34(3):635–50.

    PubMed  Google Scholar 

  31. 31.

    do Nascimento OF, Nielsen KD, Voigt M. Relationship between plantar-flexor torque generation and the magnitude of the movement-related potentials. Exp Brain Res. 2005;160(2):154–65.

    PubMed  Article  Google Scholar 

  32. 32.

    Varghese JP, Merino DM, Beyer KB, et al. Cortical control of anticipatory postural adjustments prior to stepping. Neuroscience. 2016;28(313):99–109.

    Article  CAS  Google Scholar 

  33. 33.

    da Silva Lopes. F. Neural mechanisms underlying brain waves: from neural membranes to networks. Electroencephalogr Clin Neurophysiol. 1991;79(2):81–93.

    Article  Google Scholar 

  34. 34.

    Dumermuth G, Molinari L. Spectral analysis of the EEG. Some fundamentals revisited and some open problems. Neuropsychobiology. 1987;17(1–2):85–99.

    CAS  PubMed  Google Scholar 

  35. 35.

    Bruns A, Eckhorn R. Task-related coupling from high- to low-frequency signals among visual cortical areas in human subdural recordings. Int J Psychophysiol. 2004;51(2):97–116.

    PubMed  Article  Google Scholar 

  36. 36.

    Sauseng P, Griesmayr B, Freunberger R, et al. Control mechanisms in working memory: a possible function of EEG theta oscillations. Neurosci Biobehav Rev. 2010;34(7):1015–22.

    PubMed  Article  Google Scholar 

  37. 37.

    Borich MR, Brown KE, Lakhani B, et al. Applications of electroencephalography to characterize brain activity: perspectives in stroke. J Neurol Phys Ther. 2015;39(1):43–51.

    PubMed  Article  Google Scholar 

  38. 38.

    Lopes Da Silva FH. Storm Van Leeuwen W. The cortical source of the alpha rhythm. Neurosci Lett. 1977;6(2–3):237–41.

    PubMed  Article  Google Scholar 

  39. 39.

    Baumeister J, Reinecke K, Weiss M. Changed cortical activity after anterior cruciate ligament reconstruction in a joint position paradigm: an EEG study. Scand J Med Sci Sports. 2008;18(4):473–84.

    CAS  PubMed  Article  Google Scholar 

  40. 40.

    Pfurtscheller G, Lopes da Silva FH. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol. 1999;110(11):1842–57.

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Valeriani M, Restuccia D, Di Lazzaro V, et al. Clinical and neurophysiological abnormalities before and after reconstruction of the anterior cruciate ligament of the knee. Acta Neurol Scand. 1999;99(5):303–7.

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Ochi M, Iwasa J, Uchio Y, et al. The regeneration of sensory neurones in the reconstruction of the anterior cruciate ligament. J Bone Joint Surg Br. 1999;81(5):902–6.

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Courtney CA, Rine RM. Central somatosensory changes associated with improved dynamic balance in subjects with anterior cruciate ligament deficiency. Gait Posture. 2006;24(2):190–5.

    PubMed  Article  Google Scholar 

  44. 44.

    Baumeister J, Reinecke K, Schubert M, et al. Altered electrocortical brain activity after ACL reconstruction during force control. J Orthop Res. 2011;29(9):1383–9.

    PubMed  Article  Google Scholar 

  45. 45.

    Pfurtscheller G, Brunner C, Schlogl A, et al. Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks. Neuroimage. 2006;31(1):153–9.

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Hart JM, Pietrosimone B, Hertel J, et al. Quadriceps activation following knee injuries: a systematic review. J Athl Train. 2010;45(1):87–97.

  47. 47.

    Lepley AS, Gribble PA, Thomas AC, et al. Longitudinal evaluation of stair walking biomechanics in patients with ACL injury. Med Sci Sports Exerc. 2016;48(1):7–15.

    PubMed  Article  Google Scholar 

  48. 48.

    Ingersoll CD, Grindstaff TL, Pietrosimone BG, et al. Neuromuscular consequences of anterior cruciate ligament injury. Clin Sports Med. 2008;27(3):383–404, vii.

  49. 49.

    Hart HF, Culvenor AG, Collins NJ, et al. Knee kinematics and joint moments during gait following anterior cruciate ligament reconstruction: a systematic review and meta-analysis. Br J Sports Med. 2016;50(10):597–612.

    PubMed  Article  Google Scholar 

  50. 50.

    Kobayashi T, Gamada K. Lateral ankle sprain and chronic ankle instability: a critical review. Foot Ankle Spec. 2014;7(4):298–326.

    PubMed  Article  Google Scholar 

  51. 51.

    Doherty C, Bleakley C, Hertel J, et al. Locomotive biomechanics in persons with chronic ankle instability and lateral ankle sprain copers. J Sci Med Sport. 2016;19(7):524–30.

    PubMed  Article  Google Scholar 

  52. 52.

    Doherty C, Bleakley C, Hertel J, et al. Lower extremity function during gait in participants with first time acute lateral ankle sprain compared to controls. J Electromyogr Kinesiol. 2015;25(1):182–92.

    PubMed  Article  Google Scholar 

  53. 53.

    Slemenda C, Brandt KD, Heilman DK, et al. Quadriceps weakness and osteoarthritis of the knee. Ann Intern Med. 1997;127(2):97–104.

    CAS  PubMed  Article  Google Scholar 

  54. 54.

    Mills K, Hunt MA, Ferber R. Biomechanical deviations during level walking associated with knee osteoarthritis: a systematic review and meta-analysis. Arthritis Care Res (Hoboken). 2013;65(10):1643–65.

    PubMed  Google Scholar 

  55. 55.

    Schache MB, McClelland JA, Webster KE. Lower limb strength following total knee arthroplasty: a systematic review. Knee. 2014;21(1):12–20.

    PubMed  Article  Google Scholar 

  56. 56.

    Debbi EM, Bernfeld B, Herman A, et al. Frontal plane biomechanics of the operated and non-operated knees before and after unilateral total knee arthroplasty. Clin Biomech (Bristol, Avon). 2015;30(9):889–94.

    Article  Google Scholar 

  57. 57.

    Li J, McWilliams AB, Jin Z, et al. Unilateral total hip replacement patients with symptomatic leg length inequality have abnormal hip biomechanics during walking. Clin Biomech (Bristol, Avon). 2015;30(5):513–9.

    Article  Google Scholar 

  58. 58.

    Palmieri RM, Tom JA, Edwards JE, et al. Arthrogenic muscle response induced by an experimental knee joint effusion is mediated by pre- and post-synaptic spinal mechanisms. J Electromyogr Kinesiol. 2004;14(6):631–40.

    PubMed  Article  Google Scholar 

  59. 59.

    Palmieri-Smith RM, Villwock M, Downie B, et al. Pain and effusion and quadriceps activation and strength. J Athl Train. 2013;48(2):186–91.

  60. 60.

    Hopkins JT, Ingersoll CD, Edwards JE, et al. Changes in soleus motoneuron pool excitability after artificial knee joint effusion. Arch Phys Med Rehabil. 2000;81(9):1199–203.

    CAS  PubMed  Article  Google Scholar 

  61. 61.

    Hopkins JT, Ingersoll CD, Krause BA, et al. Effect of knee joint effusion on quadriceps and soleus motoneuron pool excitability. Med Sci Sports Exerc. 2001;33(1):123–6.

    CAS  PubMed  Article  Google Scholar 

  62. 62.

    Palmieri RM, Ingersoll CD, Edwards JE, et al. Arthrogenic muscle inhibition is not present in the limb contralateral to a simulated knee joint effusion. Am J Phys Med Rehab. 2003;82(12):910–6.

    Article  Google Scholar 

  63. 63.

    Palmieri RM, Ingersoll CD, Hoffman MA, et al. Arthrogenic muscle response to a simulated ankle joint effusion. Br J Sports Med. 2004;38(1):26–30.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 64.

    Palmieri RM, Weltman A, Edwards JE, et al. Pre-synaptic modulation of quadriceps arthrogenic muscle inhibition. Knee Surg Sports Traumatol Arthrosc. 2005;13(5):370–6.

    PubMed  Article  Google Scholar 

  65. 65.

    Torry MR, Decker MJ, Millett PJ, et al. The effects of knee joint effusion on quadriceps electromyography during jogging. J Sports Sci Med. 2005;4(1):1–8.

    PubMed  PubMed Central  Google Scholar 

  66. 66.

    Klykken LW, Pietrosimone BG, Kim KM, et al. Motor-neuron pool excitability of the lower leg muscles after acute lateral ankle sprain. J Athl Train. 2011;46(3):263–9.

    PubMed  PubMed Central  Article  Google Scholar 

  67. 67.

    Lepley AS, Gribble PA, Thomas AC, et al. Quadriceps neural alterations in anterior cruciate ligament reconstructed patients: a 6-month longitudinal investigation. Scand J Med Sci Sports. 2015;25(6):828–39.

    CAS  PubMed  Article  Google Scholar 

  68. 68.

    Ward S, Pearce AJ, Pietrosimone B, et al. Neuromuscular deficits after peripheral joint injury: a neurophysiological hypothesis. Muscle Nerve. 2015;51(3):327–32.

    PubMed  Article  Google Scholar 

  69. 69.

    Kapreli E, Athanasopoulos S. The anterior cruciate ligament deficiency as a model of brain plasticity. Med Hypotheses. 2006;67(3):645–50.

    PubMed  Article  Google Scholar 

  70. 70.

    Groppa S, Oliviero A, Eisen A, et al. A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol. 2012;123(5):858–82.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  71. 71.

    Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet. 1985;1(8437):1106–7.

    CAS  PubMed  Article  Google Scholar 

  72. 72.

    Werhahn KJ, Kunesch E, Noachtar S, et al. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol. 1999;517(Pt 2):591–7.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. 73.

    Schwenkreis P, Witscher K, Janssen F, et al. Influence of the N-methyl-d-aspartate antagonist memantine on human motor cortex excitability. Neurosci Lett. 1999;270(3):137–40.

    CAS  PubMed  Article  Google Scholar 

  74. 74.

    Premoli I, Rivolta D, Espenhahn S, et al. Characterization of GABAB-receptor mediated neurotransmission in the human cortex by paired-pulse TMS-EEG. Neuroimage. 2014;103:152–62.

    CAS  PubMed  Article  Google Scholar 

  75. 75.

    Heroux ME, Tremblay F. Corticomotor excitability associated with unilateral knee dysfunction secondary to anterior cruciate ligament injury. Knee Surg Sports Traumatol Arthrosc. 2006;14(9):823–33.

    PubMed  Article  Google Scholar 

  76. 76.

    Pietrosimone BG, Lepley AS, Ericksen HM, et al. Neural excitability alterations after anterior cruciate ligament reconstruction. J Athl Train. 2015;50(6):665–74.

    PubMed  PubMed Central  Article  Google Scholar 

  77. 77.

    McLeod MM, Gribble PA, Pietrosimone BG. Chronic ankle instability and neural excitability of the lower extremity. J Athl Train. 2015;50(8):847–53.

    PubMed  PubMed Central  Article  Google Scholar 

  78. 78.

    Pietrosimone BG, Gribble PA. Chronic ankle instability and corticomotor excitability of the fibularis longus muscle. J Athl Train. 2012;47(6):621–6.

  79. 79.

    Harkey M, McLeod MM, Terada M, et al. Quadratic association between corticomotor and spinal-reflexive excitability and self-reported disability in participants with chronic ankle instability. J Sport Rehabil. 2016;25(2):137–45.

    Article  Google Scholar 

  80. 80.

    Lepley AS, Bahhur NO, Murray AM, et al. Quadriceps corticomotor excitability following an experimental knee joint effusion. Knee Surg Sports Traumatol Arthrosc. 2015;23(4):1010–7.

    PubMed  Article  Google Scholar 

  81. 81.

    Rice DA, McNair PJ, Lewis GN, et al. Quadriceps arthrogenic muscle inhibition: the effects of experimental knee joint effusion on motor cortex excitability. Arthritis Res Ther. 2014;16(6):502.

    PubMed  PubMed Central  Article  Google Scholar 

  82. 82.

    Ward SH, Pearce A, Bennell KL, et al. Quadriceps cortical adaptations in individuals with an anterior cruciate ligament injury. Knee. 2016;23(4):582–7.

    PubMed  Article  Google Scholar 

  83. 83.

    Lepley AS, Ericksen HM, Sohn DH, et al. Contributions of neural excitability and voluntary activation to quadriceps muscle strength following anterior cruciate ligament reconstruction. Knee. 2014;21(3):736–42.

    PubMed  Article  Google Scholar 

  84. 84.

    Kittelson AJ, Thomas AC, Kluger BM, et al. Corticospinal and intracortical excitability of the quadriceps in patients with knee osteoarthritis. Exp Brain Res. 2014;232(12):3991–9.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. 85.

    Rice DA, Graven-Nielsen T, Lewis GN, et al. The effects of experimental knee pain on lower limb corticospinal and motor cortex excitability. Arthritis Res Ther. 2015;17(1):204.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  86. 86.

    Needle AR, Palmer JA, Kesar TM, et al. Brain regulation of muscle tone in healthy and functionally unstable ankles. J Sport Rehabil. 2013;22(3):202–11.

    PubMed  Article  Google Scholar 

  87. 87.

    Pietrosimone BG, Lepley AS, Ericksen HM, et al. Quadriceps strength and corticospinal excitability as predictors of disability after anterior cruciate ligament reconstruction. J Sport Rehabil. 2013;22(1):1–6.

    PubMed  Article  Google Scholar 

  88. 88.

    Duclay J, Pasquet B, Martin A, et al. Specific modulation of corticospinal and spinal excitabilities during maximal voluntary isometric, shortening and lengthening contractions in synergist muscles. J Physiol. 2011;589(Pt 11):2901–16.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  89. 89.

    Obata H, Sekiguchi H, Nakazawa K, et al. Enhanced excitability of the corticospinal pathway of the ankle extensor and flexor muscles during standing in humans. Exp Brain Res. 2009;197(3):207–13.

    PubMed  Article  Google Scholar 

  90. 90.

    Gollub RL, Rauch SL. Neuroimaging: issues of design, resolution, and interpretation. Harv Rev Psychiatry. 1996;3(5):285–9.

  91. 91.

    Schultz SK. Principles of neural science. 4th ed. Washington, D.C.: Amer Psychiatric Press, Inc.; 2001.

    Google Scholar 

  92. 92.

    Friston KJ, Frith CD, Turner R, et al. Characterizing evoked hemodynamics with fMRI. Neuroimage. 1995;2(2):157–65.

    CAS  PubMed  Article  Google Scholar 

  93. 93.

    Buchel C, Holmes AP, Rees G, et al. Characterizing stimulus-response functions using nonlinear regressors in parametric fMRI experiments. Neuroimage. 1998;8(2):140–8.

    CAS  PubMed  Article  Google Scholar 

  94. 94.

    Poldrack RA, Mumford JA, Nichols TE. Handbook of functional MRI data analysis. Cambridge: Cambridge University Press; 2011.

    Book  Google Scholar 

  95. 95.

    Brown GG, Mathalon DH, Stern H, et al. Multisite reliability of cognitive BOLD data. Neuroimage. 2011;54(3):2163–75.

    PubMed  Article  Google Scholar 

  96. 96.

    Ball T, Schreiber A, Feige B, et al. The role of higher-order motor areas in voluntary movement as revealed by high-resolution EEG and fMRI. Neuroimage. 1999;10(6):682–94.

    CAS  PubMed  Article  Google Scholar 

  97. 97.

    Grooms D, Schussler E, Miller M, et al. Brain neuroplastic hip and knee control changes in ACL reconstructed individuals. J Athl Train. 2014;49(3S):S-1-S-290.

  98. 98.

    Grooms D PS, Larsen D, Chaudhari A, Onate J. Cerebral control of jump landing in anterior cruciate ligament reconstructed individuals. J Athl Training. 2015;50(6 Suppl):S-925.

  99. 99.

    Grooms DR, Page SJ, Nichols-Larsen DS, et al. Neuroplasticity associated with anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther. 2016;5:1–27.

    Google Scholar 

  100. 100.

    Swanik CB, Covassin T, Stearne DJ, et al. The relationship between neurocognitive function and noncontact anterior cruciate ligament injuries. Am J Sports Med. 2007;35(6):943–8.

    PubMed  Article  Google Scholar 

  101. 101.

    Harpham JA, Mihalik JP, Littleton AC, et al. The effect of visual and sensory performance on head impact biomechanics in college football players. Ann Biomed Eng. 2014;42(1):1–10.

    PubMed  Article  Google Scholar 

  102. 102.

    Anderson KM. Movement control and cortical activation in functional ankle instability [Dissertation]. Minnesota: University of Minnesota; 2008.

    Google Scholar 

  103. 103.

    Linortner P, Jehna M, Johansen-Berg H, et al. Aging associated changes in the motor control of ankle movements in the brain. Neurobiol Aging. 2014;35(10):2222–9.

    PubMed  PubMed Central  Article  Google Scholar 

  104. 104.

    Goble DJ, Coxon JP, Van Impe A, et al. Brain activity during ankle proprioceptive stimulation predicts balance performance in young and older adults. J Neurosci. 2011;31(45):16344–52.

    CAS  PubMed  Article  Google Scholar 

  105. 105.

    Pruim RH, Mennes M, Buitelaar JK, et al. Evaluation of ICA-AROMA and alternative strategies for motion artifact removal in resting state fMRI. Neuroimage. 2015;15(112):278–87.

    Article  Google Scholar 

  106. 106.

    Fabbri-Destro M, Rizzolatti G. Mirror neurons and mirror systems in monkeys and humans. Physiology (Bethesda). 2008;23:171–9.

    PubMed  Article  Google Scholar 

  107. 107.

    Morin O, Grezes J. What is “mirror” in the premotor cortex? A review. Neurophysiol Clin. 2008;38(3):189–95.

    CAS  PubMed  Article  Google Scholar 

  108. 108.

    Molenberghs P, Cunnington R, Mattingley JB. Is the mirror neuron system involved in imitation? A short review and meta-analysis. Neurosci Biobehav Rev. 2009;33(7):975–80.

    PubMed  Article  Google Scholar 

  109. 109.

    Wang C, Wai Y, Kuo B, et al. Cortical control of gait in healthy humans: an fMRI study. J Neural Transm. 2008;115(8):1149–58.

    PubMed  Article  Google Scholar 

  110. 110.

    Bezzola L, Merillat S, Jancke L. The effect of leisure activity golf practice on motor imagery: an fMRI study in middle adulthood. Front Hum Neurosci. 2012;6:67.

    PubMed  PubMed Central  Article  Google Scholar 

  111. 111.

    Haller S, Cunningham G, Laedermann A, et al. Shoulder apprehension impacts large-scale functional brain networks. AJNR Am J Neuroradiol. 2014;35(4):691–7.

    CAS  PubMed  Article  Google Scholar 

  112. 112.

    Cunningham G, Zanchi D, Emmert K, et al. Neural correlates of clinical scores in patients with anterior shoulder apprehension. Med Sci Sports Exerc. 2015;47(12):2612–20.

    PubMed  Article  Google Scholar 

  113. 113.

    Turella L, Pierno AC, Tubaldi F, et al. Mirror neurons in humans: consisting or confounding evidence? Brain Lang. 2009;108(1):10–21.

    PubMed  Article  Google Scholar 

  114. 114.

    Mukamel R, Ekstrom AD, Kaplan J, et al. Single-neuron responses in humans during execution and observation of actions. Curr Biol. 2010;20(8):750–6.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  115. 115.

    Rizzolatti G, Fabbri-Destro M, Cattaneo L. Mirror neurons and their clinical relevance. Nat Clin Pract Neurol. 2009;5(1):24–34.

    PubMed  Article  Google Scholar 

  116. 116.

    Clark BC, Mahato NK, Nakazawa M, et al. The power of the mind: the cortex as a critical determinant of muscle strength/weakness. J Neurophysiol. 2014;112(12):3219–26.

    PubMed  PubMed Central  Article  Google Scholar 

  117. 117.

    Draganski B, Gaser C, Busch V, et al. Neuroplasticity: changes in grey matter induced by training. Nature. 2004;427(6972):311–2.

    CAS  PubMed  Article  Google Scholar 

  118. 118.

    Ansari AH, Oghabian MA, Hossein-Zadeh GA. Assessment of functional and structural connectivity between motor cortex and thalamus using fMRI and DWI. Conf Proc IEEE Eng Med Biol Soc. 2011;2011:5056–9.

    PubMed  Google Scholar 

  119. 119.

    Jones DK, Knosche TR, Turner R. White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage. 2013;73:239–54.

    PubMed  Article  Google Scholar 

  120. 120.

    Hofstetter S, Tavor I, Tzur Moryosef S, et al. Short-term learning induces white matter plasticity in the fornix. J Neurosci. 2013;33(31):12844–50.

    CAS  PubMed  Article  Google Scholar 

  121. 121.

    Imfeld A, Oechslin MS, Meyer M, et al. White matter plasticity in the corticospinal tract of musicians: a diffusion tensor imaging study. Neuroimage. 2009;46(3):600–7.

    PubMed  Article  Google Scholar 

  122. 122.

    Hoch MC, McKeon PO. Joint mobilization improves spatiotemporal postural control and range of motion in those with chronic ankle instability. J Orthop Res. 2011;29(3):326–32.

    PubMed  Article  Google Scholar 

  123. 123.

    LeClaire JE, Wikstrom EA. Massage for postural control in individuals with chronic ankle instability. Athl Train Sport Health Care. 2012;4(5):213–9.

    Article  Google Scholar 

  124. 124.

    Ross SE, Guskiewicz KM. Effect of coordination training with and without stochastic resonance stimulation on dynamic postural stability of subjects with functional ankle instability and subjects with stable ankles. Clin J Sport Med. 2006;16(4):323–8.

    PubMed  Article  Google Scholar 

  125. 125.

    Sliz D, Smith A, Wiebking C, et al. Neural correlates of a single-session massage treatment. Brain Imaging Behav. 2012;6(1):77–87.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  126. 126.

    Salansky N, Fedotchev A. Endogenous opioid peptide level changes under electrostimulation and their assessment by the EEG. Int J Neurosci. 1994;78(3–4):193–205.

    CAS  PubMed  Article  Google Scholar 

  127. 127.

    Salansky N, Fedotchev A, Bondar A. Responses of the nervous system to low frequency stimulation and EEG rhythms: clinical implications. Neurosci Biobehav Rev. 1998;22(3):395–409.

    CAS  PubMed  Article  Google Scholar 

  128. 128.

    Nizard J, Lefaucheur JP, Helbert M, et al. Non-invasive stimulation therapies for the treatment of refractory pain. Discov Med. 2012;14(74):21–31.

    PubMed  Google Scholar 

  129. 129.

    Harkey MS, Gribble PA, Pietrosimone BG. Disinhibitory interventions and voluntary quadriceps activation: a systematic review. J Athl Train. 2014;49(3):411-21.

  130. 130.

    Hart JM, Kuenze CM, Pietrosimone BG, et al. Quadriceps function in anterior cruciate ligament-deficient knees exercising with transcutaneous electrical nerve stimulation and cryotherapy: a randomized controlled study. Clin Rehabil. 2012;26(11):974–81.

    PubMed  Article  Google Scholar 

  131. 131.

    Mang CS, Clair JM, Collins DF. Neuromuscular electrical stimulation has a global effect on corticospinal excitability for leg muscles and a focused effect for hand muscles. Exp Brain Res. 2011;209(3):355–63.

    CAS  PubMed  Article  Google Scholar 

  132. 132.

    Gibbons CE, Pietrosimone BG, Hart JM, et al. Transcranial magnetic stimulation and volitional quadriceps activation. J Athl Train. 2010;45(6):570–9.

  133. 133.

    Pietrosimone B, McLeod MM, Florea D, et al. Immediate increases in quadriceps corticomotor excitability during an electromyography biofeedback intervention. J Electromyogr Kinesiol. 2015;25(2):316–22.

    PubMed  Article  Google Scholar 

  134. 134.

    Hotting K, Roder B. Beneficial effects of physical exercise on neuroplasticity and cognition. Neurosci Biobehav Rev. 2013;37(9 Pt B):2243–57.

  135. 135.

    Taube W, Gruber M, Beck S, et al. Cortical and spinal adaptations induced by balance training: correlation between stance stability and corticospinal activation. Acta Physiol (Oxf). 2007;189(4):347–58.

    CAS  PubMed  Article  Google Scholar 

  136. 136.

    Gabriel DA, Kamen G, Frost G. Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med. 2006;36(2):133–49.

    PubMed  Article  Google Scholar 

  137. 137.

    Adkins DL, Boychuk J, Remple MS, et al. Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J Appl Physiol (1985). 2006;101(6):1776–82.

  138. 138.

    Taube W, Gruber M, Gollhofer A. Spinal and supraspinal adaptations associated with balance training and their functional relevance. Acta Physiol (Oxf). 2008;193(2):101–16.

    CAS  PubMed  Article  Google Scholar 

  139. 139.

    Ronsse R, Puttemans V, Coxon JP, et al. Motor learning with augmented feedback: modality-dependent behavioral and neural consequences. Cereb Cortex. 2011;21(6):1283–94.

    PubMed  Article  Google Scholar 

  140. 140.

    Wulf G. Attentional focus and motor learning: a review of 15 years. Int Rev Sport Exerc P. 2013;6(1):77-104.

  141. 141.

    Benjaminse A, Otten E. ACL injury prevention, more effective with a different way of motor learning? Knee Surg Sports Traumatol Arthrosc. 2011;19(4):622–7.

    PubMed  Article  Google Scholar 

  142. 142.

    Seidler RD. Neural correlates of motor learning, transfer of learning, and learning to learn. Exerc Sport Sci Rev. 2010;38(1):3–9.

    PubMed  PubMed Central  Article  Google Scholar 

  143. 143.

    Hikosaka O, Nakamura K, Sakai K, et al. Central mechanisms of motor skill learning. Curr Opin Neurobiol. 2002;12(2):217–22.

    CAS  PubMed  Article  Google Scholar 

  144. 144.

    Schilaty ND, Nagelli C, Hewett TE. Use of objective neurocognitive measures to assess the psychological states that influence return to sport following injury. Sports Med. 2016;46(3):299–303.

    PubMed  PubMed Central  Article  Google Scholar 

  145. 145.

    Grooms D, Appelbaum G, Onate J. Neuroplasticity following anterior cruciate ligament injury: a framework for visual-motor training approaches in rehabilitation. J Orthop Sports Phys Ther. 2015;45(5):381–93.

    PubMed  Article  Google Scholar 

  146. 146.

    Wikstrom EA, Brown CN. Minimum reporting standards for copers in chronic ankle instability research. Sports Med. 2014;44(2):251–68.

    PubMed  Article  Google Scholar 

  147. 147.

    Rosenthal MD, Moore JH, Stoneman PD, et al. Neuromuscular excitability changes in the vastus medialis following anterior cruciate ligament reconstruction. Electromyogr Clin Neurophysiol. 2009;49(1):43–51.

  148. 148.

    Karim H, Fuhrman SI, Sparto P, et al. Functional brain imaging of multi-sensory vestibular processing during computerized dynamic posturography using near-infrared spectroscopy. Neuroimage. 2013;1(74):318–25.

    Article  Google Scholar 

  149. 149.

    Totaro R, Barattelli G, Quaresima V, et al. Evaluation of potential factors affecting the measurement of cerebrovascular reactivity by near-infrared spectroscopy. Clin Sci (Lond). 1998;95(4):497–504.

    CAS  PubMed  Article  Google Scholar 

  150. 150.

    Miyai I, Tanabe HC, Sase I, et al. Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage. 2001;14(5):1186–92.

    CAS  PubMed  Article  Google Scholar 

  151. 151.

    Strangman G, Culver JP, Thompson JH, et al. A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage. 2002;17(2):719–31.

    PubMed  Article  Google Scholar 

  152. 152.

    Fitzgerald PB, Fountain S, Daskalakis ZJ. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol. 2006;117(12):2584–96.

    PubMed  Article  Google Scholar 

  153. 153.

    Poreisz C, Boros K, Antal A, et al. Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients. Brain Res Bull. 2007;72(4–6):208–14.

    PubMed  Article  Google Scholar 

  154. 154.

    Lotze M, Laubis-Herrmann U, Topka H. Combination of TMS and fMRI reveals a specific pattern of reorganization in M1 in patients after complete spinal cord injury. Restor Neurol Neurosci. 2006;24(2):97–107.

    CAS  PubMed  Google Scholar 

  155. 155.

    Hamzei F, Liepert J, Dettmers C, et al. Two different reorganization patterns after rehabilitative therapy: an exploratory study with fMRI and TMS. Neuroimage. 2006;31(2):710–20.

    PubMed  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Alan R. Needle.

Ethics declarations

Funding

This paper represents an independent effort of the authors with no contributions from external funding sources.

Conflicts of interest

The analysis was conducted objectively. Alan Needle, Adam Lepley, and Dustin Grooms have no potential conflicts of interest relevant to the content of this review.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Needle, A.R., Lepley, A.S. & Grooms, D.R. Central Nervous System Adaptation After Ligamentous Injury: a Summary of Theories, Evidence, and Clinical Interpretation. Sports Med 47, 1271–1288 (2017). https://doi.org/10.1007/s40279-016-0666-y

Download citation

Keywords

  • Anterior Cruciate Ligament
  • Transcranial Magnetic Stimulation
  • Motor Cortex
  • Anterior Cruciate Ligament Injury
  • Somatosensory Cortex