European Journal of Applied Physiology

, Volume 119, Issue 9, pp 2041–2052 | Cite as

Decreased supraspinal control and neuromuscular function controlling the ankle joint in athletes with chronic ankle instability

  • Ampika Nanbancha
  • Jarugool TretriluxanaEmail author
  • Weerawat Limroongreungrat
  • Komsak Sinsurin
Original Article



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.


Ankle sprains Chronic ankle instability Cortical plasticity Corticomotor excitability Neuromuscular function Supraspinal control 



Chronic ankle instability


Non-chronic ankle instability


Tibialis anterior


Peroneus longus


Gastrocnemius medialis




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



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.

Author contributions

Ampika Nanbancha and Jarugool Tretriluxana formulate research questions, designed experiment interpreted the findings and prepared the manuscript. Ampika Nanbancha performed data collection Komsak Sinsurin, and Weerawat Limroongreungrat were involved in research design supervised and providing guidance. All authors provided critical feedback and helped shape the research, analysis, and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors report they have no potential conflict of interest.

Supplementary material

421_2019_4191_MOESM1_ESM.docx (26 kb)
Supplementary file1 (DOCX 25 kb)


  1. Ambegaonkar JP, Shultz SJ (2010) Changing filtering parameters affects lower extremity pre-landing muscle activation onset times. Sokinetics Exercise Sci 8(18):125. CrossRefGoogle Scholar
  2. 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. CrossRefGoogle Scholar
  3. 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. CrossRefGoogle Scholar
  4. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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. CrossRefGoogle Scholar
  6. Chan KW, Ding BC, Mroczek KJ (2011) Acute and chronic lateral ankle instability in the athlete. Bull NYU Hosp Jt Dis 69(1):17–26PubMedGoogle Scholar
  7. 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. CrossRefPubMedGoogle Scholar
  8. 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. CrossRefGoogle Scholar
  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. CrossRefPubMedGoogle Scholar
  10. 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. CrossRefPubMedGoogle Scholar
  11. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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. CrossRefPubMedGoogle Scholar
  13. Galvan A (2010) Neural plasticity of development and learning. Hum Brain Mapp 31(6):879–890. CrossRefPubMedGoogle Scholar
  14. 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. CrossRefPubMedGoogle Scholar
  15. 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):361–374CrossRefPubMedGoogle Scholar
  16. Hertel J (2000) Functional instability following lateral ankle sprain. Sports Med 29(5):361–371CrossRefPubMedGoogle Scholar
  17. 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. CrossRefPubMedGoogle Scholar
  18. 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. CrossRefPubMedGoogle Scholar
  19. Kaminski TW, Perrin DH, Gansneder BM (1999) Eversion strength analysis of uninjured and functionally unstable ankles. J Athl Train 34(3):239–245PubMedPubMedCentralGoogle Scholar
  20. Kandel R, Eric SHJ, Thomas JJ (2000) Principles of neural science. The motor unit and muscle action, McGraw-Hill Companies, New YorkGoogle Scholar
  21. Kapreli E, Athanasopoulos S (2006) The anterior cruciate ligament deficiency as a model of brain plasticity. Med Hypotheses 67(3):645–650. CrossRefPubMedGoogle Scholar
  22. Kobayashi M, Pascual-Leone A (2003) Transcranial magnetic stimulation in neurology. The Lancet Neurology 2(3):145–156CrossRefPubMedGoogle Scholar
  23. 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. CrossRefPubMedGoogle Scholar
  24. 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. CrossRefPubMedGoogle Scholar
  25. 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. CrossRefPubMedGoogle Scholar
  26. Maeda F, Pascual-Leone A (2003) Transcranial magnetic stimulation: studying motor neurophysiology of psychiatric disorders. Psychopharmacology 168(4):359–376. CrossRefPubMedGoogle Scholar
  27. 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. CrossRefPubMedGoogle Scholar
  28. 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):502–507CrossRefPubMedGoogle Scholar
  29. McLeod MM, Gribble PA, Pietrosimone BG (2015) Chronic ankle instability and neural excitability of the lower extremity. Journal Athl Train 50(8):847–853. CrossRefGoogle Scholar
  30. 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 57–87Google Scholar
  31. 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. CrossRefPubMedGoogle Scholar
  32. Mills KR, Nithi KA (1997) Corticomotor threshold to magnetic stimulation: normal values and repeatability. Muscle Nerve 20(5):570–576CrossRefPubMedGoogle Scholar
  33. 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. CrossRefGoogle Scholar
  34. 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 7:10Google Scholar
  35. Munn J, Beard DJ, Refshauge KM, Lee RY (2003) Eccentric muscle strength in functional ankle instability. Med Sci Sports Exerc 35(2):245–250. CrossRefPubMedGoogle Scholar
  36. 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):202–211CrossRefPubMedGoogle Scholar
  37. 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):737–748CrossRefPubMedGoogle Scholar
  38. 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. CrossRefPubMedGoogle Scholar
  39. 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):144–152CrossRefPubMedPubMedCentralGoogle Scholar
  40. Neptune RR, Wright IC, van den Bogert AJ (1999) Muscle coordination and function during cutting movements. Med Sci Sports Exerc 31(2):294–302CrossRefPubMedGoogle Scholar
  41. Pietrosimone BG, Gribble PA (2012) Chronic ankle instability and corticomotor excitability of the fibularis longus muscle. J Athl Train 47(6):621–626. CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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. CrossRefPubMedGoogle Scholar
  43. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rossini PM, Rossi S (2007) Transcranial magnetic stimulation: diagnostic, therapeutic, and research potential. Neurology 68(7):484–488. CrossRefPubMedGoogle Scholar
  45. Santello M (2005) Review of motor control mechanisms underlying impact absorption from falls. Gait Posture 21(1):85–94. CrossRefPubMedGoogle Scholar
  46. Santello M, McDonagh MJ (1998) The control of timing and amplitude of EMG activity in landing movements in humans. Exp Physiol 83(6):857–874CrossRefPubMedGoogle Scholar
  47. Santos MJ, Liu W (2008) Possible factors related to functional ankle instability. J Orthop Sports Phys Ther 38(3):150–157. CrossRefPubMedGoogle Scholar
  48. 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. CrossRefPubMedGoogle Scholar
  49. 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. CrossRefPubMedGoogle Scholar
  50. 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. CrossRefPubMedGoogle Scholar
  51. 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. CrossRefPubMedGoogle Scholar
  52. 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):164–171CrossRefPubMedGoogle Scholar
  53. 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. CrossRefPubMedGoogle Scholar
  54. Wassermann EM (2002) Variation in the response to transcranial magnetic brain stimulation in the general population. Clin Neurophysiol 113(7):1165–1171CrossRefPubMedGoogle Scholar
  55. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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):487–493PubMedPubMedCentralGoogle Scholar
  57. Yeung MS, Chan KM, So CH, Yuan WY (1994) An epidemiological survey on ankle sprain. Br J Sports Med 28(2):112–116CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Faculty of Physical TherapyMahidol UniversitySalayaThailand
  2. 2.College of Sport Science and TechnologyMahidol UniversitySalayaThailand

Personalised recommendations