Abstract
Chronic ankle instability (CAI) is characterized by persistent giving way at the ankle following an acute lateral ankle sprain and is associated with an early onset of osteoarthritis. Researchers have reported that the cutaneous afferent pathway from certain leg muscles is modified in people with CAI while in a seated position. However, we do not know if these reflex modulations persist during functional activities. The purpose of this study was to further explore sensorimotor function in patients with CAI by analyzing cutaneous reflex modulation during gait. CAI (n = 11) and uninjured control (n = 11) subjects walked on a treadmill at 4 km/h and received non-noxious sural nerve stimulations at eight different time points during the gait cycle. Net electromyographic responses from four lower leg muscles were quantified 80–120 ms after stimulation for each phase of the gait cycle and compared between groups. We found that cutaneous reflex responses between groups were largely similar from the late stance to late swing phases, but uninjured control subjects, and not CAI subjects, experienced significant suppression in the medial gastrocnemius and lateral gastrocnemius muscles during the early stance phase of the gait cycle. Our results indicate that people with CAI lack a protective unloading response in the triceps surae following high-intensity sural nerve stimulation during the early stance phase of the gait cycle. Evaluating cutaneous reflex modulations may help to identify neural alterations in the reflex pathways that contribute to functional deficits in those with CAI.
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References
Aniss AM, Gandevia SC, Burke D (1992) Reflex responses in active muscles elicited by stimulation of low-threshold afferents from the human foot. J Neurophysiol 67:1375–1384
Baken BCM, Dietz V, Duysens J (2005) Phase-dependent modulation of short latency cutaneous reflexes during walking in man. Brain Res 1031:268–275
Baken BCM, Nieuwenhuijzen P, Bastiaanse CM, Dietz V, Duysens J (2006) Cutaneous reflexes evoked during human walking are reduced when self-induced. J Physiol 570:113–124
Bronner S, Agraharasamakulam S, Ojofeitimi S (2010) Reliability and validity of electrogoniometry measurement of lower extremity movement. J Med Eng Technol 34:232–242
Buford JA, Smith JL (1990) Adaptive control for backward quadrupedal walking. II. Hindlimb muscle synergies. J Neurophysiol 64:756–766
Bullock-Saxton JE (1994) Local sensation changes and altered hip muscle function following severe ankle sprain. Phys Ther 74:17–28
Caffrey E, Docherty CL, Schrader J, Klossner J (2009) The ability of 4 single-limb hopping tests to detect functional performance deficits in individuals with functional ankle instability. J Orthop Sports Phys Ther 39:799–806. https://doi.org/10.2519/jospt.2009.3042
Chinn L, Dicharry J, Hertel J (2013) Ankle kinematics of individuals with chronic ankle instability while walking and jogging on a treadmill in shoes. Phys Ther Sport 14:232–239
Delahunt E, Monaghan K, Caulfield B (2006) Altered neuromuscular control and ankle joint kinematics during walking in subjects with functional instability of the ankle joint. Am J Sports Med 34:1970–1976
Delahunt E, Coughlan GF, Caulfield B, Nightingale EJ, Lin C, Hiller CE (2010) Inclusion criteria when investigating insufficiencies in chronic ankle instability. Med Sci Sports Exerc 42:2106–2121
Docherty CL, Arnold BL (2008) Force sense deficits in functionally unstable ankles. J Orthop Res 26:1489–1493
Doherty C, Delahunt E, Caulfield B, Hertel J, Ryan J, Bleakley C (2014) The incidence and prevalence of ankle sprain injury: a systematic review and meta-analysis of prospective epidemiological studies. Sports Med 44:123–140
Donahue MS, Docherty CL, Riley ZA (2014) Decreased fibularis reflex response during inversion perturbations in FAI subjects. J Electromyogr Kinesiol 24:84–89
Duysens J, Levin O (2010) Ankle sprains: getting off on the wrong foot. Exerc Sport Sci Rev 38:143–149
Duysens J, Trippel M, Horstmann GA, Dietz V (1990) Gating and reversal of reflexes in ankle muscles during human walking. Exp Brain Res 82:351–358
Duysens J, Tax AAM, Trippel M, Dietz V (1992) Phase-dependent reversal of reflexly induced movements during human gait. Exp Brain Res 90:404–414
Duysens J, Tax AA, Murrer L, Dietz V (1996) Backward and forward walking use different patterns of phase-dependent modulation of cutaneous reflexes in humans. J Neurophysiol 76:301–310
Feger M, Donavan L, Hart J, Hertel J (2015) Lower extremity muscle activation in patients with or without chronic ankle instability during walking. J Athl Train 50:350–357
Futatsubashi G, Sasada S, Tazoe T, Komiyama T (2013) Gain modulation of the middle latency cutaneous reflex in patients with chronic joint instability after ankle sprain. Clin Neurophysiol 124:1406–1413
Futatsubashi G, Sasada S, Ohtsuka H, Suzuki S, Komiyama T (2016) History-dependent changes in the recovery process of the middle latency cutaneous reflex gain after ankle sprain injury. Eur J Appl Physiol 116:459–470
Golditz T et al (2014) Functional ankle instability as a risk factor for osteoarthritis: using T2-mapping to analyze early cartilage degeneration in the ankle joint of young athletes. Osteoarthr Cartil 22:1377–1385
Gribble PA et al (2013) Selection criteria for patients with chronic ankle instability in controlled research: a position statement of the international ankle consortium. J Orthop Sports Phys Ther 43:585–591. https://doi.org/10.2519/jospt.2013.0303
Grüneberg C, Nieuwenhuijzen P, Duysens J (2003) Reflex responses in the lower leg following landing impact on an inverting and non-inverting platform. J Physiol 550:985–993
Haridas C, Zehr EP (2003) Coordinated interlimb compensatory responses to electrical stimulation of cutaneous nerves in the hand and foot during walking. J Neurophysiol 90:2850–2861
Hertel J (2002) Functional anatomy, pathomechanics, and pathophysiology of lateral ankle instability. J Athl Train 37:364
Hoch MC, McKeon PO, Andreatta RD (2012) Plantar vibrotactile detection deficits in adults with chronic ankle instability. Med Sci Sports Exerc 44:666–672
Hopkins JT, McLoda T, McCaw S (2007) Muscle activation following sudden ankle inversion during standing and walking. Eur J Appl Physiol 99:371–378
Hubbard-Turner T (2015) Physical activity levels in college students with chronic ankle instability. J Athl Train 50:742
Itay S, Ganel A, Horoszowski H, Farine I (1982) Clinical and functional status following lateral ankle sprains: follow-up of 90 young adults treated conservatively. Orthop Rev 11:73–76
Karlsson J, Andreasson GO (1992) The effect of external ankle support in chronic lateral ankle joint instability an electromyographic study. Am J Sports Med 20:257–261
McVey ED, Palmieri RM, Docherty CL, Zinder SM, Ingersoll CD (2005) Arthrogenic muscle inhibition in the leg muscles of subjects exhibiting functional ankle instability. Foot Ankle Int 26:1055–1061
Munn J, Beard DJ, Refshauge KM, Lee RY (2003) Eccentric muscle strength in functional ankle instability. Med Sci Sports Exerc 35:245–250
Munn J, Sullivan SJ, Schneiders AG (2010) Evidence of sensorimotor deficits in functional ankle instability: a systematic review with meta-analysis. J Sci Med Sport 13:2–12
Nishikawa T, Grabiner MD (1999) Peroneal motoneuron excitability increases immediately following application of a semirigid ankle brace. J Orthop Sports Phys Ther 29:168–176
Palmieri-Smith RM, Hopkins JT, Brown TN (2009) Peroneal activation deficits in persons with functional ankle instability. Am J Sports Med 37:982–988
Simon JE, Docherty CL (2014) Current health-related quality of life is lower in former Division I collegiate athletes than in non–collegiate athletes. Am J Sports Med 42:423–429
Simon J, Donahue M, Docherty C (2012) Development of the identification of functional ankle instability. Foot Ankle Int 33:755–763
Soboroff SH, Pappius EM, Komaroff AL (1984) Benefits, risks, and costs of alternative approaches to the evaluation and treatment of severe ankle sprain. Clin Orthop Relat Res 183:160–168
Swenson DM, Yard EE, Fields SK, Comstock RD (2009) Patterns of recurrent injuries among US high school athletes, 2005–2008. Am J Sports Med 37:1586–1593
Tax AA, van Wezel B-L, Dietz V (1995) Bipedal reflex coordination to tactile stimulation of the sural nerve during human running. J Neurophysiol 73:1947–1964
Van Wezel BMH, Ottenhoff FAM, Duysens J (1997) Dynamic control of location-specific information in tactile cutaneous reflexes from the foot during human walking. J Neurosci 17:3804–3814
Yang JF, Stein RB (1990) Phase-dependent reflex reversal in human leg muscles during walking. J Neurophysiol 63:1109–1117
Zehr EP, Stein RB (1999) What functions do reflexes serve during human locomotion? Prog Neurobiol 58:185–205
Zehr E, Komiyama T, Stein R (1997) Cutaneous reflexes during human gait: electromyographic and kinematic responses to electrical stimulation. J Neurophysiol 77:3311–3325
Zehr E, Fujita K, Stein R (1998a) Reflexes from the superficial peroneal nerve during walking in stroke subjects. J Neurophysiol 79:848–858
Zehr E, Stein R, Komiyama T (1998b) Function of sural nerve reflexes during human walking. J Physiol 507:305–314
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This work was supported by funds provided by Indiana University Graduate School and School of Public Health Bloomington Research and Creativity Committee.
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Madsen, L.P., Kitano, K., Koceja, D.M. et al. Effects of chronic ankle instability on cutaneous reflex modulation during walking. Exp Brain Res 237, 1959–1971 (2019). https://doi.org/10.1007/s00221-019-05565-4
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DOI: https://doi.org/10.1007/s00221-019-05565-4