Chronic ankle instability (CAI) alters lower extremity neuromuscular function, associated with a change in corticomotor excitability. The aim of this study was to compare corticomotor excitability and neuromuscular function of the muscles around the ankle between athletes with CAI and without CAI (non-CAI).
Nineteen CAI athletes (15 men and 4 women) and 19 non-CAI athletes (15 men and 4 women) participated (age- and sex-matched). Corticomotor excitability was measured by transcranial magnetic stimulation for the following muscles: the tibialis anterior (TA), peroneus longus (PL) and gastrocnemius medialis (GM). The resting motor threshold (rMT), motor evoked potential (MEP), and latency (Lat) were subsequently measured. Neuromuscular function was assessed with a jump test, using the EMG activity before foot contact, peak torque, and joint position sense.
The corticomotor excitability in CAI showed a lower normalized MEP in the TA (p = 0.026) and PL (p = 0.003), and longer latency in the TA (p = 0.049) and GM (p = 0.027) compared with non-CAI. The neuromuscular assessment showed CAI had less EMG activity of the PL (p < 0.001), less peak torque of the dorsiflexor (p = 0.019) muscle compared with non-CAI.
Athletes with CAI had lower corticomotor excitability in the TA and PL and a longer latency in the TA and GM muscles. Additionally, CAI demonstrated functional neuromuscular deficits by decreasing EMG activity of the PL muscle and strength of the dorsiflexor muscle. Our findings indicated maladaptation at both cortical and peripheral levels among athletes with CAI.
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Chronic ankle instability
Non-chronic ankle instability
Cumberland ankle instability tool
Maximum voluntary contraction
Transcranial magnetic stimulation
Resting motor threshold
Motor evoked potential
Central nervous system
Anterior cruciate ligament
Statistical parametric mapping
Surface electromyography for the non-invasive assessment of muscles
Ambegaonkar JP, Shultz SJ (2010) Changing filtering parameters affects lower extremity pre-landing muscle activation onset times. Sokinetics Exercise Sci 8(18):125. https://doi.org/10.3233/IES-2010-0370
Allet L, Zumstein F, Eichelberger P, Armand S, Punt IM (2017) Neuromuscular control mechanisms during single-leg jump landing in subacute ankle sprain patients: a case control study. PM & R 9(3):241–250. https://doi.org/10.1016/j.pmrj.2016.07.006
Boudreau SA, Farina D, Falla D (2010) The role of motor learning and neuroplasticity in designing rehabilitation approaches for musculoskeletal pain disorders. Man Therapy 15(5):410–414. https://doi.org/10.1016/j.math.2010.05.008
Bravo-Esteban E, Taylor J, Aleixandre M, Simon-Martinez C, Torricelli D, Pons JL, Avila-Martin G, Galan-Arriero I, Gomez-Soriano J (2017) Longitudinal estimation of intramuscular tibialis anterior coherence during subacute spinal cord injury: relationship with neurophysiological, functional and clinical outcome measures. J Neuroeng Rehabil 14(1):58. https://doi.org/10.1186/s12984-017-0271-9
Brown C, Bowser B, Simpson KJ (2012) Movement variability during single leg jump landings in individuals with and without chronic ankle instability. Clin Biomech 27(1):52–63. https://doi.org/10.1016/j.clinbiomech.2011.07.012
Chan KW, Ding BC, Mroczek KJ (2011) Acute and chronic lateral ankle instability in the athlete. Bull NYU Hosp Jt Dis 69(1):17–26
Delahunt E, Monaghan K, Caulfield B (2006) Changes in lower limb kinematics, kinetics, and muscle activity in subjects with functional instability of the ankle joint during a single leg drop jump. J Orthop Res 24(10):1991–2000. https://doi.org/10.1002/jor.20235
Doherty C, Bleakley C, Hertel J, Caulfield B, Ryan J, Delahunt E (2016) Single-leg drop landing movement strategies in participants with chronic ankle instability compared with lateral ankle sprain 'copers'. Knee Surg Sports Traumatol, Arthrosc 24(4):1049–1059. https://doi.org/10.1007/s00167-015-3852-9
Donnelly L, Donovan L, Hart JM, Hertel J (2017) Eversion strength and surface electromyography measures with and without chronic ankle instability measured in 2 positions. Foot Ankle Int 38(7):769–778. https://doi.org/10.1177/1071100717701231
Fisher BE, Piraino A, Lee YY, Smith JA, Johnson S, Davenport TE, Kulig K (2016) The effect of velocity of joint mobilization on corticospinal excitability in individuals with a history of ankle sprain. J Orthop Sports Phys Ther 46(7):562–570. https://doi.org/10.2519/jospt.2016.6602
Fox J, Docherty CL, Schrader J, Applegate T (2008) Eccentric plantar-flexor torque deficits in participants with functional ankle instability. J Athl Train 43(1):51–54. https://doi.org/10.4085/1062-6050-43.1.51
Gallasch E, Christova M, Krenn M, Kossev A, Rafolt D (2009) Changes in motor cortex excitability following training of a novel goal-directed motor task. Eur J Appl Physiol 105(1):47–54. https://doi.org/10.1007/s00421-008-0871-y
Galvan A (2010) Neural plasticity of development and learning. Hum Brain Mapp 31(6):879–890. https://doi.org/10.1002/hbm.21029
Goodall S, Howatson G, Romer L, Ross E (2014) Transcranial magnetic stimulation in sport science: a commentary. Eur J Sport Sci 14(Suppl 1):S332–340. https://doi.org/10.1080/17461391.2012.704079
Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10(5):361–374
Hertel J (2000) Functional instability following lateral ankle sprain. Sports Med 29(5):361–371
Hiller CE, Refshauge KM, Bundy AC, Herbert RD, Kilbreath SL (2006) The Cumberland ankle instability tool: a report of validity and reliability testing. Arch Phys Med Rehabil 87(9):1235–1241. https://doi.org/10.1016/j.apmr.2006.05.022
Hiller CE, Nightingale EJ, Lin CW, Coughlan GF, Caulfield B, Delahunt E (2011) Characteristics of people with recurrent ankle sprains: a systematic review with meta-analysis. Br J Sports Med 45(8):660–672. https://doi.org/10.1136/bjsm.2010.077404
Kaminski TW, Perrin DH, Gansneder BM (1999) Eversion strength analysis of uninjured and functionally unstable ankles. J Athl Train 34(3):239–245
Kandel R, Eric SHJ, Thomas JJ (2000) Principles of neural science. The motor unit and muscle action, McGraw-Hill Companies, New York
Kapreli E, Athanasopoulos S (2006) The anterior cruciate ligament deficiency as a model of brain plasticity. Med Hypotheses 67(3):645–650. https://doi.org/10.1016/j.mehy.2006.01.063
Kobayashi M, Pascual-Leone A (2003) Transcranial magnetic stimulation in neurology. The Lancet Neurology 2(3):145–156
Kosik KB, Terada M, Drinkard CP, McCann RS, Gribble PA (2017) Potential corticomotor plasticity in those with and without chronic ankle instability. Med Sci Sports Exerc 49(1):141–149. https://doi.org/10.1249/MSS.0000000000001066
Lepley AS, Ericksen HM, Sohn DH, Pietrosimone BG (2014) Contributions of neural excitability and voluntary activation to quadriceps muscle strength following anterior cruciate ligament reconstruction. Knee 21(3):736–742. https://doi.org/10.1016/j.knee.2014.02.008
Li Y, Ko J, Walker MA, Brown CN, Schmidt JD, Kim SH, Simpson KJ (2018) Does chronic ankle instability influence lower extremity muscle activation of females during landing? J Electromyogr Kinesiol 38:81–87. https://doi.org/10.1016/j.jelekin.2017.11.009
Maeda F, Pascual-Leone A (2003) Transcranial magnetic stimulation: studying motor neurophysiology of psychiatric disorders. Psychopharmacology 168(4):359–376. https://doi.org/10.1007/s00213-002-1216-x
Masse-Alarie H, Beaulieu LD, Preuss R, Schneider C (2016) Corticomotor control of lumbar multifidus muscles is impaired in chronic low back pain: concurrent evidence from ultrasound imaging and double-pulse transcranial magnetic stimulation. Exp Brain Res 234(4):1033–1045. https://doi.org/10.1007/s00221-015-4528-x
Matsunaga K, Uozumi T, Tsuji S, Murai Y (1998) Age-dependent changes in physiological threshold asymmetries for the motor evoked potential and silent period following transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 109(6):502–507
McLeod MM, Gribble PA, Pietrosimone BG (2015) Chronic ankle instability and neural excitability of the lower extremity. Journal Athl Train 50(8):847–853. https://doi.org/10.4085/1062-6050-50.4.06
Mezzarane RA, Elias LA, Magalhães FH, Chaud VM, Kohn AF (2013) Experimental and simulated EMG responses in the study of the human spinal cord. In: Turker H (ed) Electrodiagnosis in new frontiers of clinical research. Intech, Rijeka, pp 57–87
Mileva KN, Bowtell JL, Kossev AR (2009) Effects of low-frequency whole-body vibration on motor-evoked potentials in healthy men. Exp Physiol 94(1):103–116. https://doi.org/10.1113/expphysiol.2008.042689
Mills KR, Nithi KA (1997) Corticomotor threshold to magnetic stimulation: normal values and repeatability. Muscle Nerve 20(5):570–576
Monaghan K, Delahunt E, Caulfield B (2006) Ankle function during gait in patients with chronic ankle instability compared to controls. Clin Biomech 21(2):168–174. https://doi.org/10.1016/j.clinbiomech.2005.09.004
Mrdakovic V, Ilic DB, Jankovic N, Rajkovic Z, Stefanovic D (2008) Pre-activity modulation of lower extremity muscles within different types and heights of deep jump. J Sports Sci Med 7:10
Munn J, Beard DJ, Refshauge KM, Lee RY (2003) Eccentric muscle strength in functional ankle instability. Med Sci Sports Exerc 35(2):245–250. https://doi.org/10.1249/01.MSS.0000048724.74659.9F
Needle AR, Palmer JA, Kesar TM, Binder-Macleod SA, Swanik CB (2013) Brain regulation of muscle tone in healthy and functionally unstable ankles. J Sport Rehabil 22(3):202–211
Needle AR, Baumeister J, Kaminski TW, Higginson JS, Farquhar WB, Swanik CB (2014a) Neuromechanical coupling in the regulation of muscle tone and joint stiffness. Scand J Med Sci Sports 24(5):737–748
Needle AR, Swanik CB, Schubert M, Reinecke K, Farquhar WB, Higginson JS, Kaminski TW, Baumeister J (2014b) Decoupling of laxity and cortical activation in functionally unstable ankles during joint loading. Eur J Appl Physiol 114(10):2129–2138. https://doi.org/10.1007/s00421-014-2929-3
Negahban H, Moradi-Bousari A, Naghibi S, Sarrafzadeh J, Shaterzadeh-Yazdi MJ, Goharpey S, Etemadi M, Mazaheri M, Feizi A (2013) The eccentric torque production capacity of the ankle, knee, and hip muscle groups in patients with unilateral chronic ankle instability. Asian J Sports Med 4(2):144–152
Neptune RR, Wright IC, van den Bogert AJ (1999) Muscle coordination and function during cutting movements. Med Sci Sports Exerc 31(2):294–302
Pietrosimone BG, Gribble PA (2012) Chronic ankle instability and corticomotor excitability of the fibularis longus muscle. J Athl Train 47(6):621–626. https://doi.org/10.4085/1062-6050-47.6.11
Robinson MA, Vanrenterghem J, Pataky TC (2015) Statistical parametric mapping (SPM) for alpha-based statistical analyses of multi-muscle EMG time-series. J Electromyogr Kinesiol 25(1):14–19. https://doi.org/10.1016/j.jelekin.2014.10.018
Rossi S, Hallett M, Rossini PM, Pascual-Leone A, Safety of TMSCG (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120(12):2008–2039. https://doi.org/10.1016/j.clinph.2009.08.016
Rossini PM, Rossi S (2007) Transcranial magnetic stimulation: diagnostic, therapeutic, and research potential. Neurology 68(7):484–488. https://doi.org/10.1212/01.wnl.0000250268.13789.b2
Santello M (2005) Review of motor control mechanisms underlying impact absorption from falls. Gait Posture 21(1):85–94. https://doi.org/10.1016/j.gaitpost.2004.01.005
Santello M, McDonagh MJ (1998) The control of timing and amplitude of EMG activity in landing movements in humans. Exp Physiol 83(6):857–874
Santos MJ, Liu W (2008) Possible factors related to functional ankle instability. J Orthop Sports Phys Ther 38(3):150–157. https://doi.org/10.2519/jospt.2008.2524
Sefton JM, Hicks-Little CA, Hubbard TJ, Clemens MG, Yengo CM, Koceja DM, Cordova ML (2008) Segmental spinal reflex adaptations associated with chronic ankle instability. Arch Phys Med Rehabil 89(10):1991–1995. https://doi.org/10.1016/j.apmr.2008.03.014
Sekir U, Yildiz Y, Hazneci B, Ors F, Aydin T (2007) Effect of isokinetic training on strength, functionality and proprioception in athletes with functional ankle instability. Knee Surg Sports Traumatol Arthrosc 15(5):654–664. https://doi.org/10.1007/s00167-006-0108-8
Son SJ, Kim H, Seeley MK, Hopkins JT (2017) Movement strategies among groups of chronic ankle instability, coper, and control. Med Sci Sports Exerc 49(8):1649–1661. https://doi.org/10.1249/MSS.0000000000001255
Suda EY, Amorim CF, Sacco Ide C (2009) Influence of ankle functional instability on the ankle electromyography during landing after volleyball blocking. J Electromyogr Kinesiol 19(2):e84–93. https://doi.org/10.1016/j.jelekin.2007.10.007
van der Kamp W, Zwinderman AH, Ferrari MD, van Dijk JG (1996) Cortical excitability and response variability of transcranial magnetic stimulation. J Clin Neurophysiol 13(2):164–171
Ward S, Pearce AJ, Pietrosimone B, Bennell K, Clark R, Bryant AL (2015) Neuromuscular deficits after peripheral joint injury: a neurophysiological hypothesis. Muscle Nerve 51(3):327–332. https://doi.org/10.1002/mus.24463
Wassermann EM (2002) Variation in the response to transcranial magnetic brain stimulation in the general population. Clin Neurophysiol 113(7):1165–1171
Webster KA, Pietrosimone BG, Gribble PA (2016) Muscle Activation During Landing Before and After Fatigue in Individuals With or Without Chronic Ankle Instability. J Athl Train 51(8):629–636. https://doi.org/10.4085/1062-6050-51.10.01
Willems T, Witvrouw E, Verstuyft J, Vaes P, De Clercq D (2002) Proprioception and Muscle Strength in Subjects With a History of Ankle Sprains and Chronic Instability. J Athl Train 37(4):487–493
Yeung MS, Chan KM, So CH, Yuan WY (1994) An epidemiological survey on ankle sprain. Br J Sports Med 28(2):112–116
The Faculty of Physical Therapy and Graduated School, Mahidol University supported this study. We thank Assoc.Prof. James J. Laskin, PhD, PT, for providing helpful comments on this manuscript.
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Communicated by Lori Ann Vallis.
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Nanbancha, A., Tretriluxana, J., Limroongreungrat, W. et al. Decreased supraspinal control and neuromuscular function controlling the ankle joint in athletes with chronic ankle instability. Eur J Appl Physiol 119, 2041–2052 (2019). https://doi.org/10.1007/s00421-019-04191-w
- Ankle sprains
- Chronic ankle instability
- Cortical plasticity
- Corticomotor excitability
- Neuromuscular function
- Supraspinal control