Evidence for the specificity of intracortical inhibitory dysfunction in asymptomatic concussed athletes

Journal of Neurotrauma

Volumn 28, Issue 4, 2011, Pages 493-502

  Tremblay, Sara ^a,b   De Beaumont, Louis ^c   Lassonde, Maryse ^a,b   Théoret, Hugo ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

afferent inhibition; intracortical inhibition; somatosensory evoked potentials; sport concussions; TMS

Indexed keywords

ADULT; ARTICLE; ATHLETE; CLINICAL ARTICLE; CONCUSSION; CONTROLLED STUDY; EVOKED SOMATOSENSORY RESPONSE; HUMAN; MEDIAN NERVE; NERVE STIMULATION; NEUROPHYSIOLOGY; PRIMARY MOTOR CORTEX; SENSORIMOTOR INTEGRATION; SOMATOSENSORY STIMULATION; SPORT INJURY; TRANSCRANIAL MAGNETIC STIMULATION;

ADULT; ANALYSIS OF VARIANCE; ATHLETES; ATHLETIC INJURIES; BRAIN CONCUSSION; ELECTRIC STIMULATION; EVOKED POTENTIALS, SOMATOSENSORY; HUMANS; MALE; MEDIAN NERVE; MOTOR CORTEX; NEURAL CONDUCTION; NEURAL INHIBITION; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 79953821019     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2010.1615     Document Type: Article

References (73)

1. Abbruzzese, G., Assini, A., Buccolieri, A., Schieppati, M., and Trompetto, C (1999). Comparison of intracortical inhibition and facilitation in distal and proximal arm muscles in humans. J. Physiol. 514, 895-903. (Pubitemid 29060333)
2. Alle, H., Heidegger, T., Krivanekova, L., and Ziemann, U. (2009). Interactions between short-interval intracortical inhibition and short-latency afferent inhibition in human motor cortex. J. Physiol. 587, 5163-5176.
3. American Academy of Neurology. (1997). Practice parameter: the management of concussion in sports (summary state-ment). Report of the Quality Standards Subcommittee. Neu-rology 48, 581-585.
4. Bajbouj, M., Lisanby, S.H., Lang, U.E., Danker-Hopfe, H., Heu-ser, I., and Neu, P. (2006). Evidence for impaired cortical in-hibition in patients with unipolar major depression. Biol. Psychiatry 59, 395-400. (Pubitemid 43289217)
5. Baker, A.J., Moulton, R.J., MacMillan, V.H., and Shedden, P.M. (1993). Excitatory amino acids in cerebrospinal fluid following traumatic brain injury in humans. J. Neurosurg. 79, 369-372. (Pubitemid 23252185)
6. Bäumer, T., Pramstaller, P.P., Siebner, H.R, Schippling, S., Ha-genah, J., Peller, M., Gerloff, C., Klein, C., and Münchau, A. (2007). Sensorimotor integration is abnormal in asymptomatic Parkin mutation carriers: a TMS study. Neurology 69, 1976-1981. (Pubitemid 350145089)
7. Bendlin, B.B., Ries, M.L., Lazar, M., Alexander, A.L., Dempsey, RJ., Rowley, H.A., Sherman, J.E., and Johnson, S.C. (2008). Longitudinal changes in patients with traumatic brain injury assessed with diffusion-tensor and volumetric imaging. Neu-roimage 42, 503-514.
8. Cantu, R.C. (1996). Head injuries in sport. Br. J. Sports Med. 30, 289-296. (Pubitemid 27073060)
9. Carter, B.G, and Butt, W. (2005). Are somatosensory evoked potentials the best predictor of outcome after severe brain injury? A systematic review. Intensive Care Med. 31, 765-775. (Pubitemid 40897530)
10. Catena, R.D., van Donkelaar, P., and Chou, L.S. (2007a). Altered balance control following concussion is better detected with an attention test during gait. Gait Posture 25, 406-411. (Pubitemid 46240899)
11. Catena, RD., van Donkelaar, P., and Chou, L.S. (2007b). Cog-nitive task effects on gait stability following concussion. Exp. Brain Res. 176, 23-31. (Pubitemid 44800515)
12. Cavanaugh, J.T., Guskiewicz, K.M., Giuliani, C., Marshall, S., Mercer, V., and Stergiou, N. (2005). Detecting altered postural control after cerebral concussion in athletes with normal postural stability. Br. J. Sports Med. 39, 805-811. (Pubitemid 41564914)
13. Centers for Disease Control and Prevention. (1997). Sports-related recurrent brain injuries\United States. JAMA 277, 1190-1191.
14. Chen, R (2004). Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp. Brain Res. 154, 1-10. (Pubitemid 38134633)
15. Chen, R., Corwell, B., and Hallett, M. (1999). Modulation of motor cortex excitability by median nerve and digit stimula-tion. Exp. Brain Res. 129, 77-86. (Pubitemid 29494842)
16. Chen, R., Cros, D., Curra, A., Di Lazzaro, V., Lefaucheur, J.P., Magistris, M.R., Mills, K., Rösler, K.M., Triggs, W.J., Ugawa, Y., and Ziemann, U. (2008). The clinical diagnostic utility of transcranial magnetic stimulation: report of an IFCN com-mittee. Clin. Neurophysiol. 119, 504-532.
17. Chistyakov, A.V., Hafner, H., Soustiel, J.F., Trubnik, M., Levy, G., and Feinsod, M. (1999). Dissociation of somatosensory and motor evoked potentials in non-comatose patients after head injury. Clin. Neurophysiol. 110, 1080-1089. (Pubitemid 29278900)
18. Chistyakov, A.V., Soustiel, J.F., Hafner, H., Elron, M., and Feinsod, M. (1998). Altered excitability of the motor cortex after minor head injury revealed by transcranial magnetic stimulation. Acta. Neurochir. 140, 467-472. (Pubitemid 28312792)
19. Chistyakov, A.V., Soustiel, J.F., Hafner, H., Trubnik, M., Levy, G., and Feinsod, M. (2001). Excitatory and inhibitory corti-cospinal responses to transcranial magnetic stimulation in patients with minor to moderate head injury. J. Neurol. Neurosurg. Psychiatry 70, 580-587 (Pubitemid 32397992)
20. Cooper, R, Osselton, J.W., and Shaw, J.C. (1980). EEG Technology (3rd ed). Butterworths: London.
21. De Beaumont, L., Brisson, B., Lassonde, M., and Jolicoeur, P. (2007b). Long-term electrophysiological changes in athletes with a history of multiple concussions. Brain Inj. 21, 631-644. (Pubitemid 46993189)
22. De Beaumont, L., Lassonde, M., Leclerc, S., and Théoret, H. (2007a). Long term and cumulative effects of sports concus-sions on motor cortex inhibition. Neurosurgery 61, 329-337.
23. De Beaumont, L., Théoret, H., Mongeon, D., Messier, J., Leclerc, S., Tremblay, S., Ellemberg, D., and Lassonde, M. (2009). Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 132, 695-708.
24. Di Lazzaro, V., Oliviero, A., Pilato, F., Saturno, E., Dileone, M., Marra, C., Daniele, A., Ghirlanda, S., Gainotti, G., and Tonali, P.A. (2004). Motor cortex hyperexcitability to transcranial magnetic stimulation in Alzheimer's disease. J. Neurol. Neu-rosurg. Psychiatry 75, 555-559. (Pubitemid 38406651)
25. Di Lazzaro, V., Oliviero, A., Pilato, F., Saturno, E., Dileone, M., Marra, C., Ghirlanda, S., Ranieri, F., Gainotti, G., and Tonali, P. (2005). Neurophysiological predictors of long term response to AChE inhibitors in AD patients. J. Neurol. Neurosurg. Psychiatry 76, 1064-1069. (Pubitemid 41081276)
26. Di Lazzaro, V., Oliviero, A., Tonali, P.A., Marra, C., Daniele, A., Profice, P., Saturno, E., Pilato, F., Masullo, C., and Rothwell, J.C (2002). Non-invasive in vivo assessment of cholinergic cortical circuits in Alzheimer's disease using transcranial magnetic stimulation. Neurology 59, 392-397. (Pubitemid 34857932)
27. Di Lazzaro, V., Pilato, F., Dileone, M., Profice, P., Ranieri, F., Ricci, V., Bria, P., Tonali, P.A., and Ziemann, U. (2007). Segregating two inhibitory circuits in human motor cortex at the level of GABAA receptor subtypes: a TMS study. Clin. Neurophysiol. 118, 2207-2214. (Pubitemid 47385353)
28. Faden, A.I., Demediuk, P., Panter, S.S., and Vink, R. (1989). The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244, 798-800. (Pubitemid 19163864)
29. Fujiki, M., Hikawa, T., Abe, T., Ishii, K., and Kobayashi, H. (2006). Reduced short latency afferent inhibition in diffuse axonal injury patients with memory impairment. Neurosci. Lett. 405, 226-230. (Pubitemid 44189721)
30. Giza, C.C., and Hovda, D.A. (2001). The neurometabolic cascade of concussion. J. Athl. Train. 36, 228-235. (Pubitemid 33685230)
31. Guskiewicz, K.M., Ross, S.E., and Marshall, S.W. (2001). Postural stability and neuropsychological deficits after concussion in collegiate athletes. J. Athl. Train. 36, 263-273. (Pubitemid 33685236)
32. Henry, L.C., Tremblay, S., Boulanger, Y., Ellenberg, D., and Lassonde, M. (2010). Neurometabolic changes in the acute phase after sports concussions. J. Neurotrauma 27, 65-76.
33. Ilic, T.V., Meintzschel, F., Cleff, U., Ruge, D., Kessler, K.R., and Ziemann, U. (2002). Short-interval paired-pulse inhibition and facilitation of human motor cortex: the dimension of stimulus intensity. J. Physiol. 545, 153-167. (Pubitemid 35386133)
34. Inglese, M., Makani, S., Johnson, G., Cohen, B.A., Silver, J.A., Gonen, O., and Grossman, R.I. (2005). Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study. J. Neurosurg. 103, 298-303. (Pubitemid 43193906)
35. Jotwani, V., and Harmon, K.G (2010). Postconcussion syndrome in athletes. Curr. Sports Med. Rep. 9, 21-26.
36. Katayama, Y., Becker, D.P., Tamura, T., and Hovda, D.A. (1990). Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J. Neurosurg. 73, 889-900.
37. Kessler, K.R., Ruge, D., Illic, T.V., and Ziemann, U. (2005). Short latency afferent inhibition and facilitation in patients with writer's cramp. Mov. Disord. 20, 238-242. (Pubitemid 40361131)
38. Kibby, MY., and Long, C.J. (1996). Minor head injury: attempts at clarifying the confusion. Brain Inj. 10, 159-186. (Pubitemid 26120327)
39. Kim, E., Lauterbach, E.C., Reeve, A., Arciniegas, D.B., Coburn, K.L., Mendez, M.F., Rummans, T.A., and Coffey, E.C. (2007). Neuropsychiatric complications of traumatic brain injury: a critical review of the literature (a report by the ANPA Committee on Research). J. Neuropsychiatry Clin. Neurosci. 19, 106-127. (Pubitemid 46649633)
40. Kobori, N., and Dash, P.K. (2006). Reversal of brain injuryinduced prefrontal glutamic acid decarboxylase expression and working memory deficits by D1 receptor antagonism J. Neurosci. 26, 4236-4246. (Pubitemid 44315383)
41. Kraus, M.F., Susmaras, T., Caughlin, B.P., Walker, C.J., Sweeney, J.A., and Little, D.M. (2007). White matter integrity and cognition in chronic traumatic brain injury: a diffusion tensor imaging study. Brain 130, 2508-2519. (Pubitemid 47511721)
42. Kujirai, T., Caramia, M.D., Rothwell, J.C., Day, B.L., Thompson, P.D., Ferbert, A., Wroe, S., Asselman, P., and Marsden, C.D. (1993). Corticocortical inhibition in human motor cortex. J. Physiol. 471, 501-519. (Pubitemid 23345592)
43. Lew, H.L., Dikmen, S., Slimp, J., Temkin, N., Lee, E.H., Newell, D., and Robinson, L.R (2003). Use of somatosensory-evoked potentials and cognitive event-related potentials in predicting outcomes of patients with severe traumatic brain injury. Am. J. Phys. Med. Rehabil. 82, 53-61. (Pubitemid 36043764)
44. Lipton, M.L., Gellella, E., Lo, C., Gold, T., Ardekani, B.A., Shifteh, K., Bello, J.A., and Branch, C.A. (2008). Multifocal white matter ultrastructural abnormalities in mild traumatic brain injury with cognitive disability: a voxel-wise analysis of dif-fusion tensor imaging. J. Neurotrauma 25, 1335-1342.
45. Maeda, F., Keenan, J.P., and Pascual-Leone, A. (2000). Inter-hemispheric asymmetry of motor cortical excitability in major depression as measured by transcranial magnetic stimulation. Br. J. Psychiatry 177, 169-173. (Pubitemid 30624830)
46. Maller, J.J., Thomson, R.H., Lewis, P.M., Rose, S.E., Pannek, K., and Fitzgerald, P.B. (2010). Traumatic brain injury, major de-pression, and diffusion tensor imaging: making connections. Brain Res. Rev. 64, 213-240.
47. Maroon, J.C., Lovell, M.R., Norwig, J., Podell, K., Powell, J.W., and Hartl, R (2000). Cerebral concussion in athletes: evaluation and neuropsychological testing. Neurosurgery 47, 659-672. (Pubitemid 32044713)
48. McCrory, P., Johnston, K., Meeuwisse, W., Aubry, M., Cantu R., Dvorak, J, Graf-Baumann, T., Kelly, J., Lovell, M., and Scha-masch, P. (2005). Summary and agreement statement of the 2nd International Conference on Concussion in Sport, Prague 2004. Clin. J. Sport. Med. 15, 48-55. (Pubitemid 40462876)
49. McDonnell, M.N., Orekhov, Y., and Ziemann, U. (2006). The role of GABA(B) receptors in intracortical inhibition in the human motor cortex. Exp. Brain Res. 173, 86-93. (Pubitemid 44099702)
50. McKee, A.C., Cantu, RC., Nowinski, C.J., Hedley-Whyte, E.T., Gavett, B.E., Budson, A.E., Santini, V.E., Lee, H.S., Kubilus, C.A., and Stern, RA. (2009). Chronic traumatic encephalopa-thy in athletes: progressive tauopathy after repetitive head injury. J. Neuropathol. Exp. Neurol. 68, 709-735.
51. Miles, L., Grossman, RI., Johnson, G., Babb, J.S., Diller, L., and Inglese, M. (2008). Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Inj. 22, 115-122. (Pubitemid 351233920)
52. Nakamura, H., Kitagawa, H., Kawaguchi, Y., and Tsuji, H. (1997). Intracortical facilitation and inhibition after tran-scranial magnetic stimulation in conscious humans. J. Physiol. 498, 817-823. (Pubitemid 27089476)
53. Orth, M., Amann, B., Robertson, M.M., and Rothwell, J.C. (2005). Excitability of motor cortex inhibitory circuits in Tourette syndrome before and after single dose nicotine. Brain 128, 1292-1300. (Pubitemid 40826183)
54. Palmer, A.M., Marion, D.W., Botscheller, M.L., Bowen, D.M., and DeKosky, S.T. (1994). Increased transmitter amino acid concentration in human ventricular CSF after brain trauma. Neuroreport 6, 153-156.
55. Parker, T.M., Osternig, L.R., Van Donkelaar, P., and Chou, L.S. (2006). Gait stability following concussion. Med. Sci. Sports. Exerc 38, 1032-1040. (Pubitemid 43902482)
56. Parker, T.M., Osternig, L.R., van Donkelaar, P., and Chou, L.S. (2007). Recovery of cognitive and dynamic motor function following concussion. Br. J. Sports Med. 41, 868-873. (Pubitemid 350232794)
57. Pascual, J.M., Solivera, J., Prieto, R, Barrios, L., López- Larrubia, P., Cerdán, S., and Roda, J.M. (2007). Time course of early metabolic changes following diffuse traumatic brain injury in rats as detected by (1)H NMR spectroscopy. J. Neurotrauma 24, 944-959. (Pubitemid 47015430)
58. Pirio Richardson, S., Bliem, B., Voller, B., Dang, N., and Hallett, M. (2009). Long-latency afferent inhibition during phasic fin-ger movement in focal hand dystonia. Exp Brain Res. 193,173-179.
59. Rabadi, M.H., and Jordan, B.D. (2001). The cumulative effect of repetitive concussion in sports. Clin. J. Sport Med. 11, 194-198. (Pubitemid 32667133)
60. Rappaport, M., Hemmerle, A.V., and Rappaport, M.L. (1990). Intermediate and long latency SEPs in relation to clinical disability in traumatic brain injury patients. Clin. Electro-encephalogr. 21, 188-191. (Pubitemid 20350376)
61. Reddy, C.C., and Collins, M.W. (2009). Sports concussion: management and predictors of outcome. Curr. Sports. Med. Rep. 8, 10-15.
62. Rogers, J.M., and Read, C.A. (2007). Psychiatric comorbidity following traumatic brain injury. Brain Inj. 21, 1321-1333. (Pubitemid 350253437)
63. Rossi, S., De Capua, A., Tavanti, M., Calossi, S., Polizzotto, N.R, Mantovani, A., Falzarano, V., Bossini, L., Passero, S., Bartalini, S., and Ulivelli, M. (2009). Dysfunctions of cortical excitability in drug-nä?ve posttraumatic stress disorder patients. Biol. Psychiatry 66, 54-61.
64. Rothman, S.M., and Olney, J.W. (1986). Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann. Neurol. 19, 105-111. (Pubitemid 16114163)
65. Sailer, A., Molnar, G.F., Paradiso, G., Gunraj, C.A., Lang, A.E., and Chen, R. (2003). Short and long latency afferent inhibition in Parkinson's disease. Brain 126,1883-1894. (Pubitemid 36917347)
66. Siebner, H.R, Dressnandt, J., Auer, C., and Conrad, B. (1998). Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 21,1209-1212. (Pubitemid 28355572)
67. Tokimura, H., Di, L.V., Tokimura, Y., Oliviero, A., Profice, P., Insola, A., Mazzone, P., Tonali, P., and Rothwell, J.C. (2000). Short latency inhibition of human hand motor cortex by so-matosensory input from the hand. J. Physiol. 523, 503-513. (Pubitemid 30137656)
68. Werhahn, K.J., Kunesch, E., Noachtar, S., Benecke, R., and Classen, J. (1999). Differential effects on motorcortical inhibi-tion induced by blockade of GABA uptake in humans. J. Physiol. 517, 591-597. (Pubitemid 29296371)
69. Wu, L., Goto, Y., Tanikawi, T., Kinukawa, N., and Tobimatsu, S. (2002). Different patterns of excitation and inhibition of the small hand and forearm muscles from magnetic brain stimu-lation in humans. Clin. Neurophysiol. 113, 1286-1294. (Pubitemid 34874520)
70. Yurkewicz, L., Weaver, J., Bullock, M.R, and Marshall, L.F. (2005). The effect of the selective NMDA receptor antagonist traxoprodil in the treatment of traumatic brain injury. J. Neurotrauma 22, 1428-1443. (Pubitemid 43122358)
71. Ziemann, U. (2004). TMS and drugs. Clin. Neurophysiol. 115, 1719-1729.
72. Ziemann, U., Lonnecker, S., Steinhoff, B.J., and Paulus, W. (1996). Effects of antiepileptic drugs on motor cortex excit-ability in humans: a transcranial magnetic stimulation study. Ann. Neurol. 40, 367-378. (Pubitemid 26304794)
73. Zumsteg, D., Wennberg, R., Gütling, E., and Hess, K. (2006). Whiplash and concussion: similar acute changes in middle-latency SEPs. Can. J. Neurol. Sci. 33, 379-386. (Pubitemid 44951986)