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Rapid Detection and Monitoring of Brain Injury Using Sensory-Evoked Responses

  • Jonathan A. N. FisherEmail author
  • Cristin G. WelleEmail author
Protocol
Part of the Neuromethods book series (NM, volume 139)

Abstract

There is currently a dearth of quantitative biomarkers for traumatic brain injury (TBI) that can be rapidly acquired and interpreted in active field environments. Clinical imaging, via computed tomography (CT) scan or magnetic resonance imaging (MRI), in combination with a clinical examination, is currently the “gold standard” for diagnosing TBI. These technologies, however, require extended imaging sessions and are rarely available during the peak therapeutic window following injury. Moreover, mild TBI (mTBI) often does not present with structural damage that can be detected by CT or MRI imaging. Techniques that probe neurophysiological function, however, present an opportunity to directly and rapidly assess brain health following head impact. One of the most basic roles of the CNS is to register and parse sensory stimuli from the environment. This process relies on an intricate feedback network that involves a multitude of widely distributed brain structures, and subtle perturbation in brain health can have a dramatic effect on afferent relay and processing of sensory information. In this chapter, we describe recent preclinical approaches for rapidly detecting and monitoring TBI using sensory-evoked physiological biomarkers, particularly somatosensory-evoked electrophysiological and hemodynamic responses. With an eye toward clinical implementation, we focus our discussion on measurements that can be achieved noninvasively.

Key words

Traumatic brain injury Biomarkers Somatosensory-evoked potentials Epidermal electronics Diffuse correlation spectroscopy Cerebral blood flow Animal models 

Notes

Acknowledgements

Supported by National Science Foundation awards 1541612 and 1641133 (J.A.N.F), internal recruitment funds at New York Medical College (J.A.N.F), Boettcher Webb-Waring Research Award (C.G.W.), internal recruitment funds at University of Colorado (C.G.W.).

References

  1. 1.
    Ruff R (2005) Two decades of advances in understanding of mild traumatic brain injury. J Head Trauma Rehabil 20:5–18. https://doi.org/10.1097/00001199-200501000-00003CrossRefPubMedGoogle Scholar
  2. 2.
    Lerner EB, Moscati RM (2001) The golden hour: scientific fact or medical “urban legend”? Acad Emerg Med 8:758–760. https://doi.org/10.1111/j.1553-2712.2001.tb00201.xCrossRefPubMedGoogle Scholar
  3. 3.
    Dinh MM, Bein K, Roncal S, Byrne CM, Petchell J, Brennan J (2013) Redefining the golden hour for severe head injury in an urban setting: the effect of prehospital arrival times on patient outcomes. Injury 44:606–610. https://doi.org/10.1016/j.injury.2012.01.011CrossRefPubMedGoogle Scholar
  4. 4.
    Becker DP, Miller JD, Ward JD, Greenberg RP, Young HF, Sakalas R (1977) The outcome from severe head injury with early diagnosis and intensive management. J Neurosurg 47:491–502. https://doi.org/10.3171/jns.1977.47.4.0491CrossRefPubMedGoogle Scholar
  5. 5.
    Stiver SI, Manley GT (2008) Prehospital management of traumatic brain injury. Neurosurg Focus 25:E5. https://doi.org/10.3171/FOC.2008.25.10.E5CrossRefPubMedGoogle Scholar
  6. 6.
    Steward W, Jones N, Schneider W (1999) Helmet system including at least three accelerometers and mass memory and method for recording in real-time orthogonal acceleration data of a headGoogle Scholar
  7. 7.
    Duma SM, Manoogian SJ, Bussone WR, Brolinson PG, Goforth MW, Donnenwerth JJ, Greenwald RM, Chu JJ, Crisco JJ (2005) Analysis of real-time head accelerations in collegiate football players. Clin J Sport Med 15:3CrossRefPubMedGoogle Scholar
  8. 8.
    Ouckama R, Pearsall DJ (2011) Evaluation of a flexible force sensor for measurement of helmet foam impact performance. J Biomech 44:904–909. https://doi.org/10.1016/j.jbiomech.2010.11.035CrossRefPubMedGoogle Scholar
  9. 9.
    Dimitriadis SI, Zouridakis G, Rezaie R, Babajani-Feremi A, Papanicolaou AC (2015) Functional connectivity changes detected with magnetoencephalography after mild traumatic brain injury. Neuroimage Clin 9:519–531. https://doi.org/10.1016/j.nicl.2015.09.011CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Dunkley BT, Da Costa L, Bethune A, Jetly R, Pang EW, Taylor MJ, Doesburg SM (2015) Low-frequency connectivity is associated with mild traumatic brain injury. Neuroimage Clin 7:611–621. https://doi.org/10.1016/j.nicl.2015.02.020CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Alhourani A, Wozny TA, Krishnaswamy D, Pathak S, Walls SA, Ghuman AS, Krieger DN, Okonkwo DO, Richardson RM, Niranjan A (2016) Magnetoencephalography-based identification of functional connectivity network disruption following mild traumatic brain injury. J Neurophysiol 116:1840–1847. https://doi.org/10.1152/jn.00513.2016CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Mayer AR, Mannell MV, Ling J, Gasparovic C, Yeo RA (2011) Functional connectivity in mild traumatic brain injury. Hum Brain Mapp 32:1825–1835. https://doi.org/10.1002/hbm.21151CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Sharp DJ, Beckmann CF, Greenwood R, Kinnunen KM, Bonnelle V, De Boissezon X, Powell JH, Counsell SJ, Patel MC, Leech R (2011) Default mode network functional and structural connectivity after traumatic brain injury. Brain 134:2233–2247. https://doi.org/10.1093/brain/awr175CrossRefPubMedGoogle Scholar
  14. 14.
    Chiu C-C, Liao Y-E, Yang L-Y, Wang J-Y, Tweedie D, Karnati HK, Greig NH, Wang J-Y (2016) Neuroinflammation in animal models of traumatic brain injury. J Neurosci Methods 272:38–49. https://doi.org/10.1016/j.jneumeth.2016.06.018CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Karve IP, Taylor JM, Crack PJ (2016) The contribution of astrocytes and microglia to traumatic brain injury. Br J Pharmacol 173:692–702. https://doi.org/10.1111/bph.13125CrossRefPubMedGoogle Scholar
  16. 16.
    Katayama Y, Becker DP, Tamura T, Hovda DA (1990) Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury. J Neurosurg 73:889–900. https://doi.org/10.3171/jns.1990.73.6.0889CrossRefPubMedGoogle Scholar
  17. 17.
    Nilsson P, Hillered L, Pontén U, Ungerstedt U (1990) Changes in cortical extracellular levels of energy-related metabolites and amino acids following concussive brain injury in rats. J Cereb Blood Flow Metab 10:631–637. https://doi.org/10.1038/jcbfm.1990.115CrossRefPubMedGoogle Scholar
  18. 18.
    Prado GR, Ross JD, DeWeerth SP, LaPlaca MC (2005) Mechanical trauma induces immediate changes in neuronal network activity. J Neural Eng 2:148. https://doi.org/10.1088/1741-2560/2/4/011CrossRefPubMedGoogle Scholar
  19. 19.
    Goforth PB, Ren J, Schwartz BS, Satin LS (2011) Excitatory synaptic transmission and network activity are depressed following mechanical injury in cortical neurons. J Neurophysiol 105:2350–2363. https://doi.org/10.1152/jn.00467.2010CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Nag S, Manias JL, Stewart DJ (2009) Pathology and new players in the pathogenesis of brain edema. Acta Neuropathol (Berl) 118:197–217. https://doi.org/10.1007/s00401-009-0541-0CrossRefGoogle Scholar
  21. 21.
    Donkin JJ, Vink R (2010) Mechanisms of cerebral edema in traumatic brain injury: therapeutic developments. Curr Opin Neurol 23:293–299. https://doi.org/10.1097/WCO.0b013e328337f451CrossRefPubMedGoogle Scholar
  22. 22.
    Corps KN, Roth TL, McGavern DB (2015) Inflammation and neuroprotection in traumatic brain injury. JAMA Neurol 72:355–362. https://doi.org/10.1001/jamaneurol.2014.3558CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Lozano D, Gonzales-Portillo GS, Acosta S, de la Pena I, Tajiri N, Kaneko Y, Borlongan CV (2015) Neuroinflammatory responses to traumatic brain injury: etiology, clinical consequences, and therapeutic opportunities. Neuropsychiatr Dis Treat 11:97–106. https://doi.org/10.2147/NDT.S65815CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Papa L, Brophy GM, Welch RD, Lewis LM, Braga CF, Tan CN, Ameli NJ, Lopez MA, Haeussler CA, Mendez Giordano DI, Silvestri S, Giordano P, Weber KD, Hill-Pryor C, Hack DC (2016) Time course and diagnostic accuracy of glial and neuronal blood biomarkers GFAP and UCH-L1 in a large cohort of trauma patients with and without mild traumatic brain injury. JAMA Neurol 73:551–560. https://doi.org/10.1001/jamaneurol.2016.0039CrossRefPubMedGoogle Scholar
  25. 25.
    Bogoslovsky T, Wilson D, Chen Y, Hanlon D, Gill J, Jeromin A, Song L, Moore C, Gong Y, Kenney K, Diaz-Arrastia R (2017) Increases of plasma levels of glial fibrillary acidic protein, Tau, and amyloid β up to 90 days after traumatic brain injury. J Neurotrauma 34:66–73. https://doi.org/10.1089/neu.2015.4333CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Goldstein LE, Fisher AM, Tagge CA, Zhang X-L, Velisek L, Sullivan JA, Upreti C, Kracht JM, Ericsson M, Wojnarowicz MW, Goletiani CJ, Maglakelidze GM, Casey N, Moncaster JA, Minaeva O, Moir RD, Nowinski CJ, Stern RA, Cantu RC, Geiling J, Blusztajn JK, Wolozin BL, Ikezu T, Stein TD, Budson AE, Kowall NW, Chargin D, Sharon A, Saman S, Hall GF, Moss WC, Cleveland RO, Tanzi RE, Stanton PK, McKee AC (2012) Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci Transl Med 4:134ra60. https://doi.org/10.1126/scitranslmed.3003716CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Daneshvar DH, Goldstein LE, Kiernan PT, Stein TD, McKee AC (2015) Post-traumatic neurodegeneration and chronic traumatic encephalopathy. Mol Cell Neurosci 66:81–90. https://doi.org/10.1016/j.mcn.2015.03.007CrossRefPubMedGoogle Scholar
  28. 28.
    Chen J, Xu X-M, Xu ZC, Zhang JH (2012) Electrophysiological approaches in traumatic brain injury—Springer. Humana, New YorkGoogle Scholar
  29. 29.
    Trudeau DL, Anderson J, Hansen LM, Shagalov DN, Schmoller J, Nugent S, Barton S (1998) Findings of mild traumatic brain injury in combat veterans with PTSD and a history of blast concussion. J Neuropsychiatry Clin Neurosci 10:308–313. https://doi.org/10.1176/jnp.10.3.308CrossRefPubMedGoogle Scholar
  30. 30.
    Thatcher RW, North DM, Curtin RT, Walker RA, Biver CJ, Gomez JF, Salazar AM (2014) An EEG severity index of traumatic brain injury. http://neuro.psychiatryonline.org/doi/10.1176/jnp.13.1.77. Accessed 24 Feb 2015
  31. 31.
    Nuwer MR, Hovda DA, Schrader LM, Vespa PM (2005) Routine and quantitative EEG in mild traumatic brain injury. Clin Neurophysiol 116:2001–2025. https://doi.org/10.1016/j.clinph.2005.05.008CrossRefPubMedGoogle Scholar
  32. 32.
    Naunheim RS, Treaster M, English J, Casner T, Chabot R (2010) Use of brain electrical activity to quantify traumatic brain injury in the emergency department. Brain Inj 24:1324–1329. https://doi.org/10.3109/02699052.2010.506862CrossRefPubMedGoogle Scholar
  33. 33.
    Ayaz SI, Thomas C, Kulek A, Tolomello R, Mika V, Robinson D, Medado P, Pearson C, Prichep LS, O’Neil BJ (2015) Comparison of quantitative EEG to current clinical decision rules for head CT use in acute mild traumatic brain injury in the ED. Am J Emerg Med 33:493–496. https://doi.org/10.1016/j.ajem.2014.11.015CrossRefPubMedGoogle Scholar
  34. 34.
    Prichep LS, Naunheim R, Bazarian J, Mould WA, Hanley D (2015) Identification of hematomas in mild traumatic brain injury using an index of quantitative brain electrical activity. J Neurotrauma 32:17–22. https://doi.org/10.1089/neu.2014.3365CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    O’Neil B, Prichep LS, Naunheim R, Chabot R (2012) Quantitative brain electrical activity in the initial screening of mild traumatic brain injuries. West J Emerg Med 13:394–400. https://doi.org/10.5811/westjem.2011.12.6815CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Rapp PE, Keyser DO, Albano A, Hernandez R, Gibson DB, Zambon RA, Hairston WD, Hughes JD, Krystal A, Nichols AS (2015) Traumatic brain injury detection using electrophysiological methods. Front Hum Neurosci 9:11. https://doi.org/10.3389/fnhum.2015.00011CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Hanley D, Prichep LS, Badjatia N, Bazarian J, Chiacchierini R, Curley KC, Garrett J, Jones E, Naunheim R, O’Neil B, O’Neill J, Wright DW, Huff JS (2017) A brain electrical activity (EEG)-based biomarker of functional impairment in traumatic brain injury: a multi-site validation trial. J Neurotrauma 35:41–47. https://doi.org/10.1089/neu.2017.5004CrossRefPubMedGoogle Scholar
  38. 38.
    Gaetz M (2004) The neurophysiology of brain injury. Clin Neurophysiol 115:4–18. https://doi.org/10.1016/S1388-2457(03)00258-XCrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Walser H, Emre M, Janzer R (1986) Somatosensory evoked potentials in comatose patients: correlation with outcome and neuropathological findings. J Neurol 233:34–40. https://doi.org/10.1007/BF00313989CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Carter BG, 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. https://doi.org/10.1007/s00134-005-2633-1CrossRefPubMedGoogle Scholar
  41. 41.
    Paxinos G, Franklin KBJ (2004) The mouse brain in stereotaxic coordinates. Gulf Professional Publishing, AmsterdamGoogle Scholar
  42. 42.
    Fisher J, Huang S, Ye M, Nabili M, Wilent W, Krauthamer V, Myers M, Welle C (2016) Real-time detection and monitoring of acute brain injury utilizing evoked electroencephalographic potentials. IEEE Trans Neural Syst Rehabil Eng 24:1003–1012. https://doi.org/10.1109/TNSRE.2016.2529663CrossRefPubMedGoogle Scholar
  43. 43.
    Huang S, Fisher JAN, Ye M, Kim YS, Ma R, Nabili M, Krauthamer V, Myers MR, Coleman TP, Welle CG (2017) Epidermal electrode technology for detecting ultrasonic perturbation of sensory brain activity. IEEE Trans Biomed Eng. https://doi.org/10.1109/TBME.2017.2713647
  44. 44.
    Jang H, Huang S, Hammer DX, Wang L, Rafi H, Ye M, Welle CG, Fisher JAN (2017) Alterations in neurovascular coupling following acute traumatic brain injury. Neurophotonics 4:045007. https://doi.org/10.1117/1.NPh.4.4.045007CrossRefPubMedGoogle Scholar
  45. 45.
    Takechi U, Matsunaga K, Nakanishi R, Yamanaga H, Murayama N, Mafune K, Tsuji S (2014) Longitudinal changes of motor cortical excitability and transcallosal inhibition after subcortical stroke. Clin Neurophysiol 125:2055–2069. https://doi.org/10.1016/j.clinph.2014.01.034CrossRefPubMedGoogle Scholar
  46. 46.
    Schwarzbach E, Bonislawski DP, Xiong G, Cohen AS (2006) Mechanisms underlying the inability to induce area CA1 LTP in the mouse after traumatic brain injury. Hippocampus 16:541–550. https://doi.org/10.1002/hipo.20183CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    DeWitt DS, Prough DS, Taylor CL, Whitley JM (1992) Reduced cerebral blood flow, oxygen delivery, and electroencephalographic activity after traumatic brain injury and mild hemorrhage in cats. J Neurosurg 76:812–821. https://doi.org/10.3171/jns.1992.76.5.0812CrossRefPubMedGoogle Scholar
  48. 48.
    McIntosh TK, Vink R, Noble L, Yamakami I, Fernyak S, Soares H, Faden AL (1989) Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28:233–244. https://doi.org/10.1016/0306-4522(89)90247-9CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Werner C, Engelhard K (2007) Pathophysiology of traumatic brain injury. Br J Anaesth 99:4–9. https://doi.org/10.1093/bja/aem131CrossRefGoogle Scholar
  50. 50.
    Toth P, Szarka N, Farkas E, Ezer E, Czeiter E, Amrein K, Ungvari Z, Hartings JA, Buki A, Koller A (2016) Traumatic brain injury-induced autoregulatory dysfunction and spreading depression-related neurovascular uncoupling: pathomechanisms, perspectives, and therapeutic implications. Am J Physiol Heart Circ Physiol 311:H1118–H1131. https://doi.org/10.1152/ajpheart.00267.2016CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Dietrich WD, Alonso O, Halley M (1994) Early microvascular and neuronal consequences of traumatic brain injury: a light and electron microscopic study in rats. J Neurotrauma 11:289–301. https://doi.org/10.1089/neu.1994.11.289CrossRefPubMedGoogle Scholar
  52. 52.
    Yi J-H, Hazell AS (2006) Excitotoxic mechanisms and the role of astrocytic glutamate transporters in traumatic brain injury. Neurochem Int 48:394–403. https://doi.org/10.1016/j.neuint.2005.12.001CrossRefPubMedGoogle Scholar
  53. 53.
    Herculano-Houzel S (2011) Scaling of brain metabolism with a fixed energy budget per neuron: implications for neuronal activity, plasticity and evolution. PLoS One 6:e17514. https://doi.org/10.1371/journal.pone.0017514CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Vavilala MS, Farr CK, Watanitanon A, Clark-Bell BC, Chandee T, Moore A, Armstead W (2017) Early changes in cerebral autoregulation among youth hospitalized after sports-related traumatic brain injury. Brain Inj 32:269–275. https://doi.org/10.1080/02699052.2017.1408145CrossRefPubMedGoogle Scholar
  55. 55.
    Albalawi T, Hamner JW, Lapointe M, Meehan WP, Tan CO (2017) The relationship between cerebral vasoreactivity and post-concussive symptom severity. J Neurotrauma 34:2700–2705. https://doi.org/10.1089/neu.2017.5060CrossRefPubMedGoogle Scholar
  56. 56.
    Zeiler FA, Cardim D, Donnelly J, Menon D, Czosnyka M, Smieleweski P (2017) Transcranial Doppler systolic flow index and ICP derived cerebrovascular reactivity indices in TBI. J Neurotrauma 35:314–322. https://doi.org/10.1089/neu.2017.5364CrossRefPubMedGoogle Scholar
  57. 57.
    Ziegler D, Cravens G, Poche G, Gandhi R, Tellez M (2017) Use of transcranial Doppler in patients with severe traumatic brain injuries. J Neurotrauma 34:121–127. https://doi.org/10.1089/neu.2015.3967CrossRefPubMedGoogle Scholar
  58. 58.
    Buxton RB, Wong EC, Frank LR (1998) Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn Reson Med 39:855–864. https://doi.org/10.1002/mrm.1910390602CrossRefPubMedGoogle Scholar
  59. 59.
    Niskanen J-P, Airaksinen AM, Sierra A, Huttunen JK, Nissinen J, Karjalainen PA, Pitkänen A, Gröhn OH (2013) Monitoring functional impairment and recovery after traumatic brain injury in rats by fMRI. J Neurotrauma 30:546–556. https://doi.org/10.1089/neu.2012.2416CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    D’Esposito M, Deouell LY, Gazzaley A (2003) Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat Rev Neurosci 4:863–872. https://doi.org/10.1038/nrn1246CrossRefPubMedGoogle Scholar
  61. 61.
    Durduran T, Yodh AG (2014) Diffuse correlation spectroscopy for non-invasive, micro-vascular cerebral blood flow measurement. Neuroimage 85(Part 1):51–63. https://doi.org/10.1016/j.neuroimage.2013.06.017CrossRefPubMedGoogle Scholar
  62. 62.
    Durduran T, Burnett MG, Yu G, Zhou C, Furuya D, Yodh AG, Detre JA, Greenberg JH (2004) Spatiotemporal quantification of cerebral blood flow during functional activation in rat somatosensory cortex using laser-speckle Flowmetry. J Cereb Blood Flow Metab 24:518–525. https://doi.org/10.1097/00004647-200405000-00005CrossRefPubMedGoogle Scholar
  63. 63.
    Zhou C, Yu G, Furuya D, Greenberg J, Yodh A, Durduran T (2006) Diffuse optical correlation tomography of cerebral blood flow during cortical spreading depression in rat brain. Opt Express 14:1125. https://doi.org/10.1364/OE.14.001125CrossRefPubMedGoogle Scholar
  64. 64.
    Zhou C, Eucker SA, Durduran T, Yu G, Ralston J, Friess SH, Ichord RN, Margulies SS, Yodh AG (2009) Diffuse optical monitoring of hemodynamic changes in piglet brain with closed head injury. J Biomed Opt 14:034015. https://doi.org/10.1117/1.3146814CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Kim D-H, Lu N, Ma R, Kim Y-S, Kim R-H, Wang S, Wu J, Won SM, Tao H, Islam A, Yu KJ, Kim T-I, Chowdhury R, Ying M, Xu L, Li M, Chung H-J, Keum H, McCormick M, Liu P, Zhang Y-W, Omenetto FG, Huang Y, Coleman T, Rogers JA (2011) Epidermal electronics. Science 333:838–843. https://doi.org/10.1126/science.1206157CrossRefPubMedGoogle Scholar
  66. 66.
    Kang DY, Kim Y-S, Ornelas G, Sinha M, Naidu K, Coleman TP (2015) Scalable microfabrication procedures for adhesive-integrated flexible and stretchable electronic sensors. Sensors 15:23459–23476. https://doi.org/10.3390/s150923459CrossRefPubMedGoogle Scholar
  67. 67.
    Gil-da-Costa R, Fung R, Kim S, Mesa D, Ma R, Kang D, Bajema M, Albright TD, Coleman TP (2013) A novel method to assess event-related brain potentials in clinical domains using frontal epidermal electronics sensors. In: Society of Neuroscience Proceedings, San Diego, CAGoogle Scholar
  68. 68.
    Coleman TP, Ma R, Fung R, Bajema M, Albright TD, Rogers J, Gil-da-Costa R (2012) Epidermal electronics capture of event-related brain potentials (ERP) signal in a “real-world” target detection task. In: Society of Neuroscience Proceedings, New Orleans, LAGoogle Scholar
  69. 69.
    Harbert MJ, Rosenberg SS, Mesa D, Sinha M, Karanjia NP, Nespeca M, Coleman TP (2013) Demonstration of the use of epidermal electronics in neurological monitoring. Wiley-Blackwell, Hoboken, pp S76–S77Google Scholar
  70. 70.
    Duncan CC, Summers AC, Perla EJ, Coburn KL, Mirsky AF (2011) Evaluation of traumatic brain injury: brain potentials in diagnosis, function, and prognosis. Int J Psychophysiol 82:24–40. https://doi.org/10.1016/j.ijpsycho.2011.02.013CrossRefPubMedGoogle Scholar
  71. 71.
    Larson MJ, Kaufman DAS, Schmalfuss IM, Perlstein WM (2007) Performance monitoring, error processing, and evaluative control following severe TBI. J Int Neuropsychol Soc 13:961–971. https://doi.org/10.1017/S1355617707071305CrossRefPubMedGoogle Scholar
  72. 72.
    Larson MJ, Fair JE, Farrer TJ, Perlstein WM (2011) Predictors of performance monitoring abilities following traumatic brain injury: the influence of negative affect and cognitive sequelae. Int J Psychophysiol 82:61–68. https://doi.org/10.1016/j.ijpsycho.2011.02.001CrossRefPubMedGoogle Scholar
  73. 73.
    Lew HL, Dikmen S, Slimp J, Temkin N, Lee EH, Newell D, Robinson LR (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 Assoc Acad Physiatr 82:53–61.; quiz 62–64, 80. https://doi.org/10.1097/01.PHM.0000043771.90606.81CrossRefGoogle Scholar
  74. 74.
    Houlden DA, Taylor AB, Feinstein A, Midha R, Bethune AJ, Stewart CP, Schwartz ML (2010) Early somatosensory evoked potential grades in comatose traumatic brain injury patients predict cognitive and functional outcome. Crit Care Med 38:167–174. https://doi.org/10.1097/CCM.0b013e3181c031b3CrossRefPubMedGoogle Scholar
  75. 75.
    Xu W, Jiang G, Chen Y, Wang X, Jiang X (2012) Prediction of minimally conscious state with somatosensory evoked potentials in long-term unconscious patients after traumatic brain injury. J Trauma Acute Care Surg 72:1024–1029. https://doi.org/10.1097/TA.0b013e31824475ccCrossRefPubMedGoogle Scholar
  76. 76.
    Schorl M, Valerius-Kukula S-J, Kemmer TP (2014) Median-evoked somatosensory potentials in severe brain injury: does initial loss of cortical potentials exclude recovery? Clin Neurol Neurosurg 123:25–33. https://doi.org/10.1016/j.clineuro.2014.05.004CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PhysiologyNew York Medical CollegeValhallaUSA
  2. 2.Departments of Neurosurgery and BioengineeringUniversity of Colorado, DenverAuroraUSA

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