Misencoding of ankle joint angle control system via cutaneous afferents reflex pathway in chronic ankle instability.
Chronic ankle instability
Cutaneous reflex
Inversion position control
Misencoding
Journal
Experimental brain research
ISSN: 1432-1106
Titre abrégé: Exp Brain Res
Pays: Germany
ID NLM: 0043312
Informations de publication
Date de publication:
Sep 2022
Sep 2022
Historique:
received:
13
02
2022
accepted:
21
06
2022
pubmed:
29
6
2022
medline:
14
9
2022
entrez:
28
6
2022
Statut:
ppublish
Résumé
This study aimed to investigate how the cutaneous reflexes in the peroneus longus (PL) muscle are affected by changing the ankle joint position in patients with chronic ankle instability (CAI). We also investigated the correlation between the degree of reflex modulation and angle position sense of the ankle joint. The participants were 19 patients with CAI and 20 age-matched controls. Cutaneous reflexes were elicited by applying non-noxious electrical stimulation to the sural nerve at the ankle joint in the neutral standing and eversion/inversion standing positions. The suppressive middle latency cutaneous reflex (MLR; ~ 70-120 ms) and angle position sense of the ankle joint were assessed. During neutral standing, the gain of the suppressive MLR was more prominent in the CAI patients than in controls, although no significant difference was seen during 30° inversion standing. In addition, the ratios of the suppressive MLR and background electromyography in a neutral position were significantly larger than those at the 15°, 25°, and 30° inversion positions in CAI patients. No such difference was seen in control individuals. Furthermore, the correlations between reflex modulation degree and position sense error were quite different in CAI patients compared to controls. These findings suggest that the sensory-motor system was deteriorated in CAI patients due to changes in the PL cutaneous reflex pathway excitability and position sense of the ankle joint.
Identifiants
pubmed: 35764722
doi: 10.1007/s00221-022-06406-7
pii: 10.1007/s00221-022-06406-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2327-2337Subventions
Organisme : Japan Society for the Promotion of Science
ID : 16K16563
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Al Adal S, Pourkazemi F, Mackey M, Hiller C (2019) The prevalence of pain in people with chronic ankle instability: a systematic review. J Athl Train 54:662–670
pubmed: 31184959
pmcid: 6602397
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
pubmed: 1597720
Bahr R, Lian O, Bahr IA (1997) A twofold reduction in the incidence of acute ankle sprains in volleyball after the introduction of an injury prevention program: a prospective cohort study. Scand J Med Sci Sports 7:172–177
pubmed: 9200322
Baken BC, Nieuwenhuijzen PH, Bastiaanse CM, Dietz V, Duysens J (2006) Cutaneous reflexes evoked during human walking are reduced when self-induced. J Physiol 570:113–124
pubmed: 16269436
Burcal C, Wikstrom E (2016) Plantar cutaneous sensitivity with and without cognitive loading in people with chronic ankle instability, copers, and uninjured controls. J Orthop Sports Phys Ther 46:270–276
pubmed: 26813754
Burke D, Gandevia S, Macefield G (1988) Responses to passive movement of receptors in joint, skin and muscle of the human hand. J Physiol 402:347–361
pubmed: 2976823
pmcid: 1191895
Burke D, Dickson HG, Skuse NF (1991) Task-dependent changes in the responses to low-threshold cutaneous afferent volleys in the human lower limb. J Physiol 432:445–458
pubmed: 1886063
pmcid: 1181334
de Noronha M, Refshauge K, Herbert R, Kilbreath S, Hertel J (2006) Do voluntary strength, proprioception, range of motion, or postural sway predict occurrence of lateral ankle sprain? Br J Sports Med 40:824–828
pubmed: 16920769
pmcid: 2465053
dos Santos M, Gorges A, Rios J (2014) Individuals with chronic ankle instability exhibit decreased postural sway while kicking in a single-leg stance. Gait Posture 40:231–236
pubmed: 24794648
Drakos M, Domb B, Starkey C, Callahan L, Allen A (2010) Injury in the national basketball association: a 17-year overview. Sports Health 2:284–290
pubmed: 23015949
pmcid: 3445097
Duysens J, Levin O (2010) Ankle sprains: getting off on the wrong foot. Exerc Sport Sci Rev 38:143–149
pubmed: 20577063
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
pubmed: 2286237
Duysens J, Hoogkamer W, Levin O (2013) Is there “arthrogenic inhibition” of cutaneous reflexes in subjects with functional ankle instability? Clin Neurophysiol 124:1264–1266
pubmed: 23567073
Edin B (2001) Cutaneous afferents provide information about knee joint movements in humans. J Physiol 531:289–297
pubmed: 11179411
pmcid: 2278439
Fallon J, Bent L, McNulty P, Macefield V (2005) Evidence for strong synaptic coupling between single tactile afferents from the sole of the foot and motoneurons supplying leg muscles. J Neurophysiol 94:3795–3804
pubmed: 16079197
Fong D, Hong Y, Chan L, Yung P, Chan K (2007) A systematic review on ankle injury and ankle sprain in sports. Sports Med 37:73–94
pubmed: 17190537
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
pubmed: 23541471
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
pubmed: 26560108
Gandevia S, McCloskey D (1976) Joint sense, muscle sense, and their combination as position sense, measured at the distal interphalangeal joint of the middle finger. J Physiol 260:387–407
pubmed: 978533
pmcid: 1309097
Gibbs J, Harrison LM, Stephens JA (1995) Cutaneomuscular reflexes recorded from the lower limb in man during different tasks. J Physiol 487(Pt 1):237–242
pubmed: 7473252
pmcid: 1156612
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
pubmed: 12813158
pmcid: 2343073
Hertel J (2002) Functional anatomy, pathomechanics, and pathophysiology of lateral ankle instability. J Athl Train 37:364–375
pubmed: 12937557
pmcid: 164367
Hiller C, Refshauge K, Bundy A, Herbert R, Kilbreath S (2006) The Cumberland ankle instability tool: a report of validity and reliability testing. Arch Phys Med Rehabil 87:1235–1241
pubmed: 16935061
Hoch M, McKeon P (2011) Joint mobilization improves spatiotemporal postural control and range of motion in those with chronic ankle instability. J Orthop Res 29:326–332
pubmed: 20886654
Hoch M, McKeon P, Andreatta R (2012) Plantar vibrotactile detection deficits in adults with chronic ankle instability. Med Sci Sports Exerc 44:666–672
pubmed: 21959910
Hootman JM, Dick R, Agel J (2007) Epidemiology of collegiate injuries for 15 sports: summary and recommendations for injury prevention initiatives. J Athl Train 42:311–319
pubmed: 17710181
pmcid: 1941297
Johansson H, Sojka P (1985) Actions on gamma-motoneurones elicited by electrical stimulation of cutaneous afferent fibres in the hind limb of the cat. J Physiol 366:343–363
pubmed: 4057094
pmcid: 1193037
Kim JH, Kim HY, Chung K, Chung JM (2011) Responses of spinal dorsal horn neurons to foot movements in rats with a sprained ankle. J Neurophysiol 105:2043–2049
pubmed: 21389306
pmcid: 3094192
Komiyama T, Zehr EP, Stein RB (2000) Absence of nerve specificity in human cutaneous reflexes during standing. Exp Brain Res 133:267–272
pubmed: 10968228
Konradsen L (2002a) Factors contributing to chronic ankle instability: kinesthesia and joint position sense. J Athl Train 37:381–385
pubmed: 12937559
pmcid: 164369
Konradsen L (2002b) Sensori-motor control of the uninjured and injured human ankle. J Electromyogr Kinesiol 12:199–203
pubmed: 12086814
Konradsen L, Ravn JB, Sorensen AI (1993) Proprioception at the ankle: the effect of anaesthetic blockade of ligament receptors. J Bone Jt Surg Br 75:433–436
Konradsen L, Olesen S, Hansen HM (1998) Ankle sensorimotor control and eversion strength after acute ankle inversion injuries. Am J Sports Med 26:72–77
pubmed: 9474405
Kunugi S, Masunari A, Noh B, Mori T, Yoshida N, Miyakawa S (2017) Cross-cultural adaptation, reliability, and validity of the Japanese version of the Cumberland ankle instability tool. Disabil Rehabil 39:50–58
pubmed: 26878332
Lamers M, Reeves J, Alshamali R, Murnaghan C, Bent L (2019) Can texture change joint position sense at the knee joint in those with poor joint position accuracy? Somatosens Mot Res 36:230–240
pubmed: 31509053
Lephart S, Pincivero D, Rozzi S (1998) Proprioception of the ankle and knee. Sports Med 25:149–155
pubmed: 9554026
McKeon PO, Stein AJ, Ingersoll CD, Hertel J (2012) Altered plantar-receptor stimulation impairs postural control in those with chronic ankle instability. J Sport Rehabil 21:1–6
pubmed: 22318247
Michelson JD, Hutchins C (1995) Mechanoreceptors in human ankle ligaments. J Bone Jt Surg Br 77:219–224
Monaghan K, Delahunt E, Caulfield B (2006) Ankle function during gait in patients with chronic ankle instability compared to controls. Clin Biomech (bristol, Avon) 21:168–174
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
pubmed: 19442581
Nakajima T, Sakamoto M, Tazoe T, Endoh T, Komiyama T (2006) Location specificity of plantar cutaneous reflexes involving lower limb muscles in humans. Exp Brain Res 175:514–525
pubmed: 16847613
Nieuwenhuijzen P, Duysens J (2007) Proactive and reactive mechanisms play a role in stepping on inverting surfaces during gait. J Neurophysiol 98:2266–2273
pubmed: 17715190
Nieuwenhuijzen P, Grüneberg C, Duysens J (2002) Mechanically induced ankle inversion during human walking and jumping. J Neurosci Methods 117:133–140
pubmed: 12100978
Powell M, Powden C, Houston M, Hoch M (2014) Plantar cutaneous sensitivity and balance in individuals with and without chronic ankle instability. Clin J Sport Med 24:490–496
pubmed: 24451692
Santos MJ, Liu W (2007) Unloading reaction to electrical stimulation at neutral and supinated ankle positions. Gait Posture 26:106–112
pubmed: 16962780
Seki K, Perlmutter SI, Fetz EE (2003) Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat Neurosci 6:1309–1316
pubmed: 14625555
Song K, Kang T, Wikstrom E, Jun H, Lee S (2017) Effects of reduced plantar cutaneous sensation on static postural control in individuals with and without chronic ankle instability. J Sci Med Sport 20:910–914
pubmed: 28571626
Waldén M, Hägglund M, Ekstrand J (2013) Time-trends and circumstances surrounding ankle injuries in men’s professional football: an 11-year follow-up of the UEFA Champions League injury study. Br J Sports Med 47:748–753
pubmed: 23813486
Willems T, Witvrouw E, Verstuyft J, Vaes P, De Clercq D (2002) Proprioception and muscle strength in subjects with a histroy of ankle sprains and chronic instability. J Athl Train 37:487–493
pubmed: 12937572
pmcid: 164382
Willems T, Witvrouw E, Delbaere K, Philippaerts R, De Bourdeaudhuij I, De Clercq D (2005) Intrinsic risk factors for inversion ankle sprains in females–a prospective study. Scand J Med Sci Sports 15:336–345
pubmed: 16181258
Winter DA, Yack HJ (1987) EMG profiles during normal human walking: stride-to-stride and inter-subject variability. Electroencephalogr Clin Neurophysiol 67:402–411
pubmed: 2444408
Zehr EP, Stein RB (1999) What functions do reflexes serve during human locomotion? Prog Neurobiol 58:185–205
pubmed: 10338359
Zehr EP, Stein RB, Komiyama T (1998) Function of sural nerve reflexes during human walking. J Physiol 507:305–314
pubmed: 9490858
pmcid: 2230764