Using transcranial magnetic stimulation to quantify electrophysiological changes following concussive brain injury: A systematic review

Clinical and Experimental Pharmacology and Physiology

Volumn 42, Issue 4, 2015, Pages 394-405

  Major, Brendan P ^a   Rogers, Mark A ^a   Pearce, Alan J ^a  

^a DEAKIN UNIVERSITY   (Australia)

Author keywords

Concussion; Evoked potential; Mild traumatic brain injury; Systematic review; Transcranial magnetic stimulation

Indexed keywords

ARTICLE; DISEASE CLASSIFICATION; HUMAN; NERVE EXCITABILITY; NERVOUS SYSTEM ELECTROPHYSIOLOGY; POSTCONCUSSION SYNDROME; PROGNOSTIC ASSESSMENT; QUALITY CONTROL; QUANTITATIVE ANALYSIS; SYSTEMATIC REVIEW; TIME; TRANSCRANIAL MAGNETIC STIMULATION; ANIMAL; BRAIN CONCUSSION; CONVALESCENCE; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; EVOKED MUSCLE RESPONSE; MOTOR CORTEX; NERVE CELL INHIBITION; NERVE CONDUCTION; PATHOPHYSIOLOGY; PREDICTIVE VALUE; PROGNOSIS;

ANIMALS; BRAIN CONCUSSION; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; EVOKED POTENTIALS, MOTOR; HUMANS; MOTOR CORTEX; NEURAL CONDUCTION; NEURAL INHIBITION; PREDICTIVE VALUE OF TESTS; PROGNOSIS; RECOVERY OF FUNCTION; TIME FACTORS; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84925442808     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12363     Document Type: Article

References (69)

1. WHO. Neurological disorders: public health challenges. World Health Organization, New York; 2006.
2. McKee AC, Cantu RC, Nowinski CJ et al. Chronic traumatic encephalopathy in athletes: Progressive tauopathy after repetitive head injury. J. Neuropathol. Exp. Neurol. 2009; 68: 709-35.
3. Mez J, Stern RA, McKee AC. Chronic traumatic encephalopathy: Where are we and where are we going? Curr. Neurol. Neurosci. Rep. 2013; 13: 407.
4. Ropper AH, Gorson KC. Concussion. N. Engl. J. Med. 2007; 356: 166-72.
5. Daneshvar DH, Riley DO, Nowinski CJ, McKee AC, Stern RA, Cantu RC. Long-term consequences: Effects on normal development profile after concussion. Phys Med Rehabil Clin N Am. 2011; 22: 683-700, ix.
6. Jordan BD. The clinical spectrum of sport-related traumatic brain injury. Nat. Rev. Neurol. 2013; 9: 222-30.
7. Iverson GL, Gaetz M, Lovell MR, Collins MW. Cumulative effects of concussion in amateur athletes. Brain Inj. 2004; 18: 433-43.
8. McKee AC, Daneshvar DH, Alvarez VE, Stein TD. The neuropathology of sport. Acta Neuropathol. 2014; 127: 29-51.
9. McKee AC, Stern RA, Nowinski CJ et al. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013; 136 (Pt 1): 43-64.
10. Alwis DS, Johnstone V, Yan E, Rajan R. Diffuse traumatic brain injury and the sensory brain. Clin. Exp. Pharmacol. Physiol. 2013; 40: 473-83.
11. Giza CC, Hovda DA. The neurometabolic cascade of concussion. J Athl Train 2001; 36: 228.
12. Dimou S, Lagopoulos J. Towards objective markers of concussion in sport: A review of white matter and neurometabolic changes in the brain following sports-related concussion. J. Neurotrauma 2013; 31: 413-24.
13. Collie A, Darby D, Maruff P. Computerised cognitive assessment of athletes with sports related head injury. Br. J. Sports Med. 2001; 35: 297-302.
14. Grindel SH, Lovell MR, Collins MW. The assessment of sport-related concussion: The evidence behind neuropsychological testing and management. Clin. J. Sport Med. 2001; 11: 134-43.
15. McCrory P, Johnston K, Meeuwisse W et al. Summary and agreement statement of the 2nd International Conference on Concussion in Sport, Prague 2004. Br. J. Sports Med. 2005; 39: 196-204.
16. Kutcher JS, McCrory P, Davis G, Ptito A, Meeuwisse WH, Broglio SP. What evidence exists for new strategies or technologies in the diagnosis of sports concussion and assessment of recovery? Br. J. Sports Med. 2013; 47: 299-303.
17. Rabadi MH, Jordan BD. The cumulative effect of repetitive concussion in sports. Clin. J. Sport Med. 2001; 11: 194-8.
18. De Beaumont L, Lassonde M, Leclerc S, Théoret H. Long-Term and cumulative effects of sports concussion on motor cortex inhibition. Neurosurgery 2007; 61: 329-36.
19. Partridge B, Hall W. Conflicts of interest in recommendations to use computerized neuropsychological tests to manage concussion in professional football codes. Neuroethics. 2014; 7: 63-74.
20. Gilbert F, Partridge BJ. The need to tackle concussion in Australian football codes. Med. J. Aust. 2012; 196: 561.
21. Darling SR, Leddy JJ, Baker JG et al. Evaluation of the Zurich guidelines and exercise testing for return to play in adolescents following concussion. Clin. J. Sport Med. 2014; 24: 128-33.
22. Davis G, Iverson G, Guskiewicz K, Ptito A, Johnston K. Contributions of neuroimaging, balance testing, electrophysiology and blood markers to the assessment of sport-related concussion. Br. J. Sports Med. 2009; 43 (Suppl. 1): i36-45.
23. Birbaumer N, Murguialday AR, Cohen L. Brain-computer interface in paralysis. Curr. Opin. Neurol. 2008; 21: 634-8.
24. Killane I, Browett G, Reilly RB, editors. Measurement of attention during movement: Acquisition of ambulatory EEG and cognitive performance from healthy young adults. Engineering in Medicine and Biology Society (EMBC), 2013 35th Annual International Conference of the IEEE; 2013: IEEE, Osaka.
25. Hallett M. Transcranial magnetic stimulation and the human brain. Nature 2000; 406: 147-50.
26. Kobayashi M, Pascual-Leone A. Transcranial magnetic stimulation in neurology. Lancet Neurol. 2003; 2: 145-56.
27. Pearce AJ, Morris ME. Evidence base for exercise therapy in adults with neurological conditions. Cameron M, Selig S, Hemphill D, (eds). Clinical exercise for rehabilitation and functional training: A case-based approach. Elsevier Publishing, Melbourne. 2011. p. 68-83.
28. Ziemann U, Lönnecker S, Steinhoff B, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: A transcranial magnetic stimulation study. Ann. Neurol. 1996; 40: 367-78.
29. Pearce AJ, Rowe GS, Whyte DG. Neural conduction and excitability following a simple warm up. J Sci Med Sport 2012; 15: 164-8.
30. Wilson SA, Lockwood RJ, Thickbroom GW, Mastaglia FL. The muscle silent period following transcranial magnetic cortical stimulation. J. Neurol. Sci. 1993; 114: 216-22.
31. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J. Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J. Physiol. 1999; 517: 591-7.
32. Florian J, Müller-Dahlhaus M, Liu Y, Ziemann U. Inhibitory circuits and the nature of their interactions in the human motor cortex-a pharmacological TMS study. J. Physiol. 2008; 586: 495-514.
33. Ziemann U. Pharmacology of TMS measures. Wasserman E, Epstein C, Ziemann U, Walsh V, Paus T, Lisanby S (eds). The Oxford Handbook of Transcranial Stimullation. Oxford University Press, London. 2008. p. 135-51.
34. Kujirai T, Caramia M, Rothwell JC et al. Corticocortical inhibition in human motor cortex. J. Physiol. 1993; 471: 501-19.
35. Ziemann U, Chen R, Cohen LG, Hallett M. Dextromethorphan decreases the excitability of the human motor cortex. Neurology 1998; 51: 1320-4.
36. McDonnell MN, Orekhov Y, Ziemann U. Suppression of LTP-like plasticity in human motor cortex by the GABAB receptor agonist baclofen. Exp. Brain Res. 2007; 180: 181-6.
37. Benwell NM, Mastaglia FL, Thickbroom GW. Differential changes in long-interval intracortical inhibition and silent period duration during fatiguing hand exercise. Exp. Brain Res. 2007; 179: 255-62.
38. Chen R. Studies of human motor physiology with transcranial magnetic stimulation. Muscle Nerve 2000; 23 (Suppl. 9): S26-32.
39. Miller NR, Yasen AL, Maynard LF, Chou L-S, Howell DR, Christie AD. Acute and longitudinal changes in motor cortex function following mild traumatic brain injury. Brain Inj. 2014; 1-7.
40. De Beaumont L, Theoret H, Mongeon D et al. Brain function decline in healthy retired athletes who sustained their last sports concussion in early adulthood. Brain 2009; 132: 695-708.
41. Chistyakov AV, Hafner H, Soustiel JF, Trubnik M, Levy G, Feinsod M. Dissociation of somatosensory and motor evoked potentials in non-comatose patients after head injury. Clin. Neurophysiol. 1999; 110: 1080-9.
42. Livingston SC, Goodkin HP, Hertel JN, Saliba EN, Barth JT, Ingersoll CD. Differential rates of recovery after acute sport-related concussion: Electrophysiologic, symptomatic, and neurocognitive indices. J. Clin. Neurophysiol. 2012; 29: 23-32.
43. Livingston SC, Saliba EN, Goodkin HP, Barth JT, Hertel JN, Ingersoll CD. A preliminary investigation of motor evoked potential abnormalities following sport-related concussion. Brain Inj. 2010; 24: 904-13.
44. Pearce AJ, Hoy K, Rogers MA et al. The long-term effects of sports concussion on retired Australian football players: A study using Transcranial Magnetic Stimulation. J. Neurotrauma 2014; 31: 1139-45.
45. Chistyakov AV, Soustiel JF, Hafner H, Trubnik M, Levy G, Feinsod M. Excitatory and inhibitory corticospinal responses to transcranial magnetic stimulation in patients with minor to moderate head injury. J. Neurol. Neurosurg. Psychiatry 2001; 70: 580-7.
46. Tallus J, Lioumis P, Hämäläinen H, Kähkönen S, Tenovuo O. Long-lasting TMS motor threshold elevation in mild traumatic brain injury. Acta Neurol. Scand. 2012; 126: 178-82.
47. De Beaumont L, Mongeon D, Sb T et al. Persistent Motor System Abnormalities in Formerly Concussed Athletes. J. Athl. Train. 2011; 46: 234-40.
48. Tremblay S, de Beaumont L, Lassonde M, Théoret H. Evidence for the specificity of intracortical inhibitory dysfunction in asymptomatic concussed athletes. J. Neurotrauma 2011; 28: 493-502.
49. Tremblay S, Beaulé V, Proulx S et al. Multimodal assessment of primary motor cortex integrity following sport concussion in asymptomatic athletes. Clin Neurophys. 2014; 125: 1371-79.
50. Kelly JP, Rosenberg JH. Diagnosis and management of concussion in sports. Neurology 1997; 48: 575-80.
51. Assocation AMO. The management of concussion in Australian Football, Melbourne. Australian Football League, Melbourne, 2011.
52. Powers KC, Cinelli ME, Kalmar JM. Cortical hypoexcitability persists beyond the symptomatic phase of a concussion. Brain Inj. 2014; 28: 465-71.
53. Pearce AJ, Hoy K, Rogers MA et al. Acute motor, neurocognitive and neurophysiological change following concussion injury in Australian amature football. A prospective multimodal investigation. J Sci Med Sport. 2014 (In Press).
54. Eldaief MC, Press DZ, Pascual-Leone A. Transcranial magnetic stimulation in neurology A review of established and prospective applications. Neurology: Clinical. Practice 2013; 3: 519-26.
55. Chen R, Cros D, Curra A et al. The clinical diagnostic utility of transcranial magnetic stimulation: Report of an IFCN committee. Clin. Neurophysiol. 2008; 119: 504-32.
56. Brasil-Neto J, Cammarota A, Valls-Solé J, Pascual-Leone A, Hallett M, Cohen L. Role of intracortical mechanisms in the late part of the silent period to transcranial stimulation of the human motor cortex. Acta Neurol. Scand. 1995; 92: 383-6.
57. Inghilleri M, Berardelli A, Cruccu G, Manfredi M. Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J. Physiol. 1993; 466: 521-34.
58. Siebner HR, Dressnandt J, Auer C, Conrad B. Continuous intrathecal baclofen infusions induced a marked increase of the transcranially evoked silent period in a patient with generalized dystonia. Muscle Nerve 1998; 21: 1209-12.
59. McGinley M, Hoffman RL, Russ DW, Thomas JS, Clark BC. Older adults exhibit more intracortical inhibition and less intracortical facilitation than young adults. Exp. Gerontol. 2010; 45: 671-8.
60. Wolters A, Ziemann U, Benecke R. The cortical silent period. In: Wasserman E, Epstein C, Ziemann U, Walsh V, Paus T, Lisanby S. (eds). The oxford handbook of transcranial stimulation. Oxford University Press, London. 2008. p. 91-102.
61. Vucic S, Ziemann U, Eisen A, Hallett M, Kiernan MC. Transcranial magnetic stimulation and amyotrophic lateral sclerosis: Pathophysiological insights. J. Neurol. Neurosurg. Psychiatry 2013; 84: 1161-70.
62. Philpott AL, Fitzgerald PB, Cummins TD, Georgiou-Karistianis N. Transcranial magnetic stimulation as a tool for understanding neurophysiology in Huntington's disease: a review. Neurosci. Biobehav. Rev. 2013; 37: 1420-33.
63. Bajbouj M, Lisanby SH, Lang UE, Danker-Hopfe H, Heuser I, Neu P. Evidence for impaired cortical inhibition in patients with unipolar major depression. Biol. Psychiatry 2006; 59: 395-400.
64. Daskalakis ZJ, Christensen BK, Chen R, Fitzgerald PB, Zipursky RB, Kapur S. Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation. Arch. Gen. Psychiatry 2002; 59: 347-54.
65. Moher D, Liberati A, Tetzlaff J, Altman DG. Reprint-preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Phys. Ther. 2009; 89: 873-80.
66. Tallus J, Lioumis P, Hämäläinen H, Kähkönen S, Tenovuo O. Transcranial magnetic stimulation-electroencephalography responses in recovered and symptomatic mild traumatic brain injury. J. Neurotrauma 2013; 30: 1270-7.
67. Slavin RE. Best evidence synthesis: An intelligent alternative to meta-analysis. J. Clin. Epidemiol. 1995; 48: 9-18.
68. Chipchase L, Schabrun S, Cohen L et al. A checklist for assessing the methodological quality of studies using transcranial magnetic stimulation to study the motor system: An international consensus study. Clin. Neurophysiol. 2012; 123: 1698-704.
69. Corp DT, Lum JA, Tooley GA, Pearce AJ. Corticospinal activity during dual tasking: A systematic review and meta-analysis of TMS literature from 1995 to 2013. Neurosci. Biobehav. Rev. 2014; 43: 74.