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.
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References
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.
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.
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.
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.
McCluskey G, Blackburn TA. Classification of knee ligament instabilities. Phys Ther. 1980;60(12):1575–7.
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.
Valderrabano V, Hintermann B, Horisberger M, et al. Ligamentous posttraumatic ankle osteoarthritis. Am J Sports Med. 2006;34(4):612–20.
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.
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.
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.
Hopkins J, Ingersoll CD. Arthrogenic muscle inhibition: a limiting factor in joint rehabilitation. J Sport Rehabil. 2000;9(2):135–59.
Swanik CB. Brains and sprains: The brain’s role in noncontact anterior cruciate ligament injuries. J Athl Train. 2015;50(10):1100–2.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Konradsen L. Sensori-motor control of the uninjured and injured human ankle. J Electromyogr Kinesiol. 2002;12(3):199–203.
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.
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.
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.
Baumeister J. Sensorimotor control and associated brain activity in sports medicine research. Paderborn: Universitat Paderborn; 2013.
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.
Sur S, Sinha VK. Event-related potential: an overview. Ind Psychiatry J. 2009;18(1):70–3.
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.
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.
Varghese JP, Merino DM, Beyer KB, et al. Cortical control of anticipatory postural adjustments prior to stepping. Neuroscience. 2016;28(313):99–109.
da Silva Lopes. F. Neural mechanisms underlying brain waves: from neural membranes to networks. Electroencephalogr Clin Neurophysiol. 1991;79(2):81–93.
Dumermuth G, Molinari L. Spectral analysis of the EEG. Some fundamentals revisited and some open problems. Neuropsychobiology. 1987;17(1–2):85–99.
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.
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.
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.
Lopes Da Silva FH. Storm Van Leeuwen W. The cortical source of the alpha rhythm. Neurosci Lett. 1977;6(2–3):237–41.
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.
Pfurtscheller G, Lopes da Silva FH. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol. 1999;110(11):1842–57.
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.
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.
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.
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.
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.
Hart JM, Pietrosimone B, Hertel J, et al. Quadriceps activation following knee injuries: a systematic review. J Athl Train. 2010;45(1):87–97.
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.
Ingersoll CD, Grindstaff TL, Pietrosimone BG, et al. Neuromuscular consequences of anterior cruciate ligament injury. Clin Sports Med. 2008;27(3):383–404, vii.
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.
Kobayashi T, Gamada K. Lateral ankle sprain and chronic ankle instability: a critical review. Foot Ankle Spec. 2014;7(4):298–326.
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.
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.
Slemenda C, Brandt KD, Heilman DK, et al. Quadriceps weakness and osteoarthritis of the knee. Ann Intern Med. 1997;127(2):97–104.
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.
Schache MB, McClelland JA, Webster KE. Lower limb strength following total knee arthroplasty: a systematic review. Knee. 2014;21(1):12–20.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Ward S, Pearce AJ, Pietrosimone B, et al. Neuromuscular deficits after peripheral joint injury: a neurophysiological hypothesis. Muscle Nerve. 2015;51(3):327–32.
Kapreli E, Athanasopoulos S. The anterior cruciate ligament deficiency as a model of brain plasticity. Med Hypotheses. 2006;67(3):645–50.
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.
Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet. 1985;1(8437):1106–7.
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.
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.
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.
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.
Pietrosimone BG, Lepley AS, Ericksen HM, et al. Neural excitability alterations after anterior cruciate ligament reconstruction. J Athl Train. 2015;50(6):665–74.
McLeod MM, Gribble PA, Pietrosimone BG. Chronic ankle instability and neural excitability of the lower extremity. J Athl Train. 2015;50(8):847–53.
Pietrosimone BG, Gribble PA. Chronic ankle instability and corticomotor excitability of the fibularis longus muscle. J Athl Train. 2012;47(6):621–6.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Gollub RL, Rauch SL. Neuroimaging: issues of design, resolution, and interpretation. Harv Rev Psychiatry. 1996;3(5):285–9.
Schultz SK. Principles of neural science. 4th ed. Washington, D.C.: Amer Psychiatric Press, Inc.; 2001.
Friston KJ, Frith CD, Turner R, et al. Characterizing evoked hemodynamics with fMRI. Neuroimage. 1995;2(2):157–65.
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.
Poldrack RA, Mumford JA, Nichols TE. Handbook of functional MRI data analysis. Cambridge: Cambridge University Press; 2011.
Brown GG, Mathalon DH, Stern H, et al. Multisite reliability of cognitive BOLD data. Neuroimage. 2011;54(3):2163–75.
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.
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.
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.
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.
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.
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.
Anderson KM. Movement control and cortical activation in functional ankle instability [Dissertation]. Minnesota: University of Minnesota; 2008.
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.
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.
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.
Fabbri-Destro M, Rizzolatti G. Mirror neurons and mirror systems in monkeys and humans. Physiology (Bethesda). 2008;23:171–9.
Morin O, Grezes J. What is “mirror” in the premotor cortex? A review. Neurophysiol Clin. 2008;38(3):189–95.
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.
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.
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.
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.
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.
Turella L, Pierno AC, Tubaldi F, et al. Mirror neurons in humans: consisting or confounding evidence? Brain Lang. 2009;108(1):10–21.
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.
Rizzolatti G, Fabbri-Destro M, Cattaneo L. Mirror neurons and their clinical relevance. Nat Clin Pract Neurol. 2009;5(1):24–34.
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.
Draganski B, Gaser C, Busch V, et al. Neuroplasticity: changes in grey matter induced by training. Nature. 2004;427(6972):311–2.
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.
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.
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.
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.
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.
LeClaire JE, Wikstrom EA. Massage for postural control in individuals with chronic ankle instability. Athl Train Sport Health Care. 2012;4(5):213–9.
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.
Sliz D, Smith A, Wiebking C, et al. Neural correlates of a single-session massage treatment. Brain Imaging Behav. 2012;6(1):77–87.
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.
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.
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.
Harkey MS, Gribble PA, Pietrosimone BG. Disinhibitory interventions and voluntary quadriceps activation: a systematic review. J Athl Train. 2014;49(3):411-21.
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.
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.
Gibbons CE, Pietrosimone BG, Hart JM, et al. Transcranial magnetic stimulation and volitional quadriceps activation. J Athl Train. 2010;45(6):570–9.
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.
Hotting K, Roder B. Beneficial effects of physical exercise on neuroplasticity and cognition. Neurosci Biobehav Rev. 2013;37(9 Pt B):2243–57.
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.
Gabriel DA, Kamen G, Frost G. Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med. 2006;36(2):133–49.
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.
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.
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.
Wulf G. Attentional focus and motor learning: a review of 15 years. Int Rev Sport Exerc P. 2013;6(1):77-104.
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.
Seidler RD. Neural correlates of motor learning, transfer of learning, and learning to learn. Exerc Sport Sci Rev. 2010;38(1):3–9.
Hikosaka O, Nakamura K, Sakai K, et al. Central mechanisms of motor skill learning. Curr Opin Neurobiol. 2002;12(2):217–22.
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.
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.
Wikstrom EA, Brown CN. Minimum reporting standards for copers in chronic ankle instability research. Sports Med. 2014;44(2):251–68.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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This paper represents an independent effort of the authors with no contributions from external funding sources.
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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.
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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
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DOI: https://doi.org/10.1007/s40279-016-0666-y