New therapeutic options for the treatment of patients with disorders of consciousness: The field of neuromodulation

[en] Neuromodulation techniques aimed at normalizing the neurophysiologic disturbance produced by brain lesions or dysfunction have been studied for years in attempts to modulate brain activity to treat several neurological diseases. The field of (non)invasive brain stimulation offers a valuable alternative to improve the recovery of severely brain-injured patients with disorders of consciousness, a population that lacks of effective treatment options, especially at the chronic stage. We here describe invasive and noninvasive brain stimulation techniques, namely, deep brain stimulation (DBS) and transcranial direct current stimulation (tDCS), as therapeutic options for patients with DOC. DBS has shown to induce extensive behavioral improvement after the implantation of an electrical stimulator in the intralaminar nuclei in case reports. However, large controlled clinical trials have to be conducted in order to confirm the clinical benefit of this treatment. Regarding tDCS, the first studies, targeting the left prefrontal cortex, have shown encouraging results, with significant behavioral improvements, in both acute and chronic patients. Besides behavioral improvements, mechanisms underlying the effects of these neuromodulation techniques need to be further investigated. The mesocircuit model, by integrating the fronto-striato-thalamic loop, provides a conceptual foundation to explain the effects of several treatments having shown some effectiveness in the recovery of patients with DOC. © Springer International Publishing AG 2018.

Disciplines :

Neurology

Author, co-author :

Thibaut, Aurore ; Université de Liège - ULiège > GIGA : Coma Group

Schiff, N. D.; Feil Family Brain and Mind Research Institute, Weill Cornell Medical College, New York, NY, United States

Language :

English

Title :

New therapeutic options for the treatment of patients with disorders of consciousness: The field of neuromodulation

Publication date :

2017

Main work title :

Coma and Disorders of Consciousness: Second Edition

Publisher :

Springer International Publishing

Pages :

207-223

Peer reviewed :

Peer reviewed

Available on ORBi :

since 25 September 2018

Statistics

Number of views

94 (7 by ULiège)

Number of downloads

218 (9 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Voss HU, Uluc AM, Dyke JP, et al. Possible axonal regrowth in late recovery from the minimally conscious state. J Clin Invest. 2006;116:2005-11. doi:10.1172/JCI27021.
Estraneo A, Moretta P, Loreto V, et al. Late recovery after traumatic, anoxic, or hemorrhagic long-lasting vegetative state. Neurology. 2010;75:239-45. doi:10.1212/WNL.0b013e3181e8e8cc.
Bruno M-A, Ledoux D, Vanhaudenhuyse A, et al. Prognosis of patients with altered state of consciousness. Coma Disord Conscious. 2012; doi:10.1007/978-1-4471-2440-5_2.
Schiff ND, Giacino JT, Kalmar K, et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature. 2007;448:600-3. doi:10.1038/nature06041.
Schnakers C, Hustinx R, Vandewalle G, et al. Measuring the effect of amantadine in chronic anoxic minimally conscious state. J Neurol Neurosurg Psychiatry. 2008;79:225-7. doi:10.1136/ jnnp.2007.124099.
Giacino JT, Whyte J, Bagiella E, et al. Placebo-controlled trial of amantadine for severe traumatic brain injury. N Engl J Med. 2012;366:819-26. doi:10.1056/NEJMoa1102609.
Fridman EA, Calvar J, Bonetto M, et al. Fast awakening from minimally conscious state with apomorphine. Brain Inj. 2009;23:172-7. doi:10.1080/02699050802649662.
Sara M, Sacco S, Cipolla F, et al. An unexpected recovery from permanent vegetative state. Brain Inj. 2007;21:101-3. doi:10.1080/02699050601151761.
Whyte J, Rajan R, Rosenbaum A, et al. Zolpidem and restoration of consciousness. Am J Phys Med Rehabil. 2014;93:101-13. doi:10.1097/PHM.0000000000000069.
Thonnard M, Gosseries O, Demertzi A, et al. Effect of zolpidem in chronic disorders of consciousness: a prospective open-label study. Funct Neurol. 2014;28:259-64.
Jox RJ, Bernat JL, Laureys S, Racine E. Disorders of consciousness: responding to requests for novel diagnostic and therapeutic interventions. Lancet Neurol. 2012;11:732-8. doi:10.1016/ S1474-4422(12)70154-0.
Laureys S, Lemaire C, Maquet P, et al. Cerebral metabolism during vegetative state and after recovery to consciousness. J Neurol Neurosurg Psychiatry. 1999;67:121.
Laureys S, Goldman S, Phillips C, et al. Impaired effective cortical connectivity in vegetative state: preliminary investigation using PET. Neuroimage. 1999;9:377-82. doi:10.1006/nimg. 1998.0414.
Beuthien-Baumann B, Handrick W, Schmidt T, et al. Persistent vegetative state: evaluation of brain metabolism and brain perfusion with PET and SPECT. Nucl Med Commun. 2003;24:643-649. doi:10.1097/01.mnm.0000075192.18521.9d.
Juengling FD, Kassubek J, Huppertz HJ, et al. Separating functional and structural damage in persistent vegetative state using combined voxel-based analysis of 3-D MRI and FDG-PET. J Neurol Sci. 2005;228:179-84. doi:10.1016/j.jns.2004.11.052.
Nakao S, Takata S, Uemura H, et al. Relationship between Barthel Index scores during the acute phase of rehabilitation and subsequent ADL in stroke patients. J Med Investig. 2010;57:81-8.
Lull N, Noe E, Lull JJ, et al. Voxel-based statistical analysis of thalamic glucose metabolism in traumatic brain injury: relationship with consciousness and cognition. Brain Inj. 2010;24:1098-107. doi:10.3109/02699052.2010.494592.
Silva S, Alacoque X, Fourcade O, et al. Wakefulness and loss of awareness: brain and brainstem interaction in the vegetative state. Neurology. 2010;74:313-20. doi:10.1212/ WNL.0b013e3181cbcd96.
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, et al. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain. 2010;133:161-71. doi:10.1093/brain/awp313.
Thibaut A, Bruno MA, Chatelle C, et al. Metabolic activity in external and internal awareness networks in severely brain-damaged patients. J Rehabil Med. 2012;44:487-94.
D'Esposito M, Aguirre GK, Zarahn E, et al. Functional MRI studies of spatial and nonspatial working memory. Brain Res Cogn Brain Res. 1998;7:1-13.
D'Esposito M, Detre JA, Alsop DC, et al. The neural basis of the central executive system of working memory. Nature. 1995;378:279-81. doi:10.1038/378279a0.
Devinsky O, D'Esposito M. Neurology of cognitive and behavioural disorders. Oxford: Oxford University; 2004.
Lieberman MD. Social cognitive neuroscience: a review of core processes. Annu Rev Psychol. 2007;58:259-89. doi:10.1146/annurev.psych.58.110405.085654.
Thibaut A, Di Perri C, Chatelle C, et al. Clinical response to tDCS depends on residual brain metabolism and grey matter integrity in patients with minimally conscious state. Brain Stimul. 2015;8:1116-23. doi:10.1016/j.brs.2015.07.024.
Chatelle C, Thibaut A, Gosseries O, et al. Changes in cerebral metabolism in patients with a minimally conscious state responding to zolpidem. Front Hum Neurosci. 2014;8:917. doi:10.3389/fnhum.2014.00917.
Boly M, Tshibanda L, Vanhaudenhuyse A, et al. Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum Brain Mapp. 2009;30:2393-400. doi:10.1002/hbm.20672.
Silva S, de Pasquale F, Vuillaume C, et al. Disruption of posteromedial large-scale neural communication predicts recovery from coma. Neurology. 2015;85:2036-44. doi:10.1212/ WNL.0000000000002196.
Raichle ME, Snyder AZ. A default mode of brain function: a brief history of an evolving idea. Neuroimage. 2007;37:1083-9. doi:10.1016/j.neuroimage.2007.02.041.
Laureys S, Boly M, Maquet P. Tracking the recovery of consciousness from coma. J Clin Invest. 2006;116:1823-5. doi:10.1172/JCI29172.
Crone C, Nielsen J, Petersen N, et al. Disynaptic reciprocal inhibition of ankle extensors in spastic patients. Brain. 1994;117(Pt 5):1161-8.
Crone JS, Schurz M, Höller Y, et al. Impaired consciousness is linked to changes in effective connectivity of the posterior cingulate cortex within the default mode network. Neuroimage. 2015;110:101-9. doi:10.1016/j.neuroimage.2015.01.037.
Lant ND, Gonzalez-Lara LE, Owen AM, Fernández-Espejo D. Relationship between the anterior forebrain mesocircuit and the default mode network in the structural bases of disorders of consciousness. Neuroimage Clin. 2016;10:27-35. doi:10.1016/j.nicl.2015.11.004.
Beuthien-Baumann B, Handrick W, Schmidt T, et al. Persistent vegetative state: evaluation of brain metabolism and brain perfusion with PET and SPECT. Nucl Med Commun. 2003;24:643-9. doi:10.1097/01.mnm.0000075192.18521.9d.
Juengling FD, Kassubek J, Huppertz HJ, et al. Separating functional and structural damage in persistent vegetative state using combined voxel-based analysis of 3-D MRI and FDG-PET. J Neurol Sci. 2005;228:179-84. doi:10.1016/j.jns.2004.11.052.
Nakao S, Takata S, Uemura H, et al. Relationship between Barthel Index scores during the acute phase of rehabilitation and subsequent ADL in stroke patients. J Med Investig. 2010;57:81-8.
Lull N, Noe E, Lull JJ, et al. Voxel-based statistical analysis of thalamic glucose metabolism in traumatic brain injury: relationship with consciousness and cognition. Brain Inj. 2010;24:1098-107. doi:10.3109/02699052.2010.494592.
Silva S, Alacoque X, Fourcade O, et al. Wakefulness and loss of awareness: brain and brainstem interaction in the vegetative state. Neurology. 2010;74:313-20. doi:10.1212/ WNL.0b013e3181cbcd96.
Vanhaudenhuyse A, Noirhomme Q, Tshibanda LJ, et al. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain. 2010;133:161-71. doi:10.1093/brain/awp313.
Thibaut A, Bruno MA, Chatelle C, et al. Metabolic activity in external and internal awareness networks in severely brain-damaged patients. J Rehabil Med. 2012;44:487-94.
D'Esposito M, Aguirre GK, Zarahn E, et al. Functional MRI studies of spatial and nonspatial working memory. Brain Res Cogn Brain Res. 1998;7:1-13.
D'Esposito M, Detre JA, Alsop DC, et al. The neural basis of the central executive system of working memory. Nature. 1995;378:279-81. doi:10.1038/378279a0.
Devinsky O, D'Esposito M. Neurology of cognitive and behavioural disorders. Oxford: Oxford University; 2004.
Lieberman MD. Social cognitive neuroscience: a review of core processes. Annu Rev Psychol. 2007;58:259-89. doi:10.1146/annurev.psych.58.110405.085654.
Thibaut A, Di Perri C, Chatelle C, et al. Clinical response to tDCS depends on residual brain metabolism and grey matter integrity in patients with minimally conscious state. Brain Stimul. 2015;8:1116-23. doi:10.1016/j.brs.2015.07.024.
Chatelle C, Thibaut A, Gosseries O, et al. Changes in cerebral metabolism in patients with a minimally conscious state responding to zolpidem. Front Hum Neurosci. 2014;8:917. doi:10.3389/fnhum.2014.00917.
Boly M, Tshibanda L, Vanhaudenhuyse A, et al. Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum Brain Mapp. 2009;30:2393-400. doi:10.1002/hbm.20672.
Silva S, de Pasquale F, Vuillaume C, et al. Disruption of posteromedial large-scale neural communication predicts recovery from coma. Neurology. 2015;85:2036-44. doi:10.1212/ WNL.0000000000002196.
Raichle ME, Snyder AZ. A default mode of brain function: a brief history of an evolving idea. Neuroimage. 2007;37:1083-9. doi:10.1016/j.neuroimage.2007.02.041.
Laureys S, Boly M, Maquet P. Tracking the recovery of consciousness from coma. J Clin Invest. 2006;116:1823-5. doi:10.1172/JCI29172.
Crone C, Nielsen J, Petersen N, et al. Disynaptic reciprocal inhibition of ankle extensors in spastic patients. Brain. 1994;117(Pt 5):1161-8.
Crone JS, Schurz M, Höller Y, et al. Impaired consciousness is linked to changes in effective connectivity of the posterior cingulate cortex within the default mode network. Neuroimage. 2015;110:101-9. doi:10.1016/j.neuroimage.2015.01.037.
Lant ND, Gonzalez-Lara LE, Owen AM, Fernández-Espejo D. Relationship between the anterior forebrain mesocircuit and the default mode network in the structural bases of disorders of consciousness. Neuroimage Clin. 2016;10:27-35. doi:10.1016/j.nicl.2015.11.004.
Adams JH, Graham DI, Jennett B. The neuropathology of the vegetative state after an acute brain insult. Brain. 2000;123(Pt 7):1327-38.
Yamamoto T, Kobayashi K, Kasai M, et al. DBS therapy for the vegetative state and minimally conscious state. Acta Neurochir Suppl. 2005;93:101-4.
Giacino JT, Kalmar K, Whyte J. The JFK coma recovery scale-revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil. 2004;85:2020-9.
Boggio PS, Ferrucci R, Rigonatti SP, et al. Effects of transcranial direct current stimulation on working memory in patients with Parkinson's disease. J Neurol Sci. 2006;249:31-8. doi:10.1016/j.jns.2006.05.062.
Ferrucci R, Mameli F, Guidi I, et al. Transcranial direct current stimulation improves recognition memory in Alzheimer disease. Neurology. 2008;71:493-8. doi:10.1212/01.wnl. 0000317060.43722.a3.
Kang EK, Kim DY, Paik NJ. Transcranial direct current stimulation of the left prefrontal cortex improves attention in patients with traumatic brain injury: a pilot study. J Rehabil Med. 2012;44:346-50. doi:10.2340/16501977-0947.
Nelson JT, McKinley RA, Golob EJ, et al. Enhancing vigilance in operators with prefrontal cortex transcranial direct current stimulation (tDCS). Neuroimage. 2012; doi:10.1016/j. neuroimage.2012.11.061.
Antal A, Terney D, Kuhnl S, Paulus W. Anodal transcranial direct current stimulation of the motor cortex ameliorates chronic pain and reduces short intracortical inhibition. J Pain Symptom Manag. 2010;39:890-903. doi:10.1016/j.jpainsymman.2009.09.023.
Baker JM, Rorden C, Fridriksson J. Using transcranial direct-current stimulation to treat stroke patients with aphasia. Stroke. 2010;41:1229-36. doi:10.1161/STROKEAHA.109.576785.
Frank E, Schecklmann M, Landgrebe M, et al. Treatment of chronic tinnitus with repeated sessions of prefrontal transcranial direct current stimulation: outcomes from an open-label pilot study. J Neurol. 2012;259:327-33. doi:10.1007/s00415-011-6189-4.
Loo CK, Alonzo A, Martin D, et al. Transcranial direct current stimulation for depression: 3-week, randomised, sham-controlled trial. Br J Psychiatry. 2012;200:52-9. doi:10.1192/bjp. bp.111.097634.
Zaehle T, Sandmann P, Thorne JD, et al. Transcranial direct current stimulation of the prefrontal cortex modulates working memory performance: combined behavioural and electrophysiological evidence. BMC Neurosci. 2011;12:2. doi:10.1186/1471-2202-12-2.
George MS, Padberg F, Schlaepfer TE, et al. Controversy: repetitive transcranial magnetic stimulation or transcranial direct current stimulation shows efficacy in treating psychiatric diseases (depression, mania, schizophrenia, obsessive-compulsive disorder, panic, posttraumatic stress disorder). Brain Stimul. 2009;2:14-21. doi:10.1016/j.brs.2008.06.001.
Nitsche MA, Cohen LG, Wassermann EM, et al. Transcranial direct current stimulation: state of the art 2008. Brain Stimul. 2008;1:206-23. doi:10.1016/j.brs.2008.06.004.
Nitsche MA, Seeber A, Frommann K, et al. Modulating parameters of excitability during and after transcranial direct current stimulation of the human motor cortex. J Physiol. 2005;568:291-
Liebetanz D, Nitsche MA, Tergau F, Paulus W. Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. Brain. 2002;125:2238-47.
Thibaut A, Bruno MA, Ledoux D, et al. tDCS in patients with disorders of consciousness: sham-controlled randomised double blind study. Neurology. 2014;82:1112-8.
Giacino JT, Ashwal S, Childs N, et al. The minimally conscious state: definition and diagnostic criteria. Neurology. 2002;58:349-53.
Monti MM. Cognition in the vegetative state. Annu Rev Clin Psychol. 2012;8:431-54. doi:10.1146/annurev-clinpsy-032511-143050.
Castillo-Saavedra L, Gebodh N, Bikson M, et al. Clinically effective treatment of fibromyalgia pain with high-definition transcranial direct current stimulation: phase II open-label dose optimization. J Pain. 2016;17:14-26. doi:10.1016/j.jpain.2015.09.009.
Brunoni AR, Valiengo L, Baccaro A, et al. The sertraline vs. electrical current therapy for treating depression clinical study: results from a factorial, randomized, controlled trial. JAMA Psychiat. 2013;70:383-91. doi:10.1001/2013.jamapsychiatry.32.
Thibaut A, Bruno MA, Wannez S, et al. Long term effect of repeated tDCS in minimally conscious patients. Submitted.
Angelakis E, Liouta E, Andreadis N, et al. Transcranial direct current stimulation effects in disorders of consciousness. Arch Phys Med Rehabil. 2014;95:283-9. doi:10.1016/j. apmr.2013.09.002.
Laureys S, Faymonville ME, Luxen A, et al. Restoration of thalamocortical connectivity after recovery from persistent vegetative state. Lancet. 2000;355:1790-1.
Dehaene S, Sergent C, Changeux JP. A neuronal network model linking subjective reports and objective physiological data during conscious perception. Proc Natl Acad Sci U S A. 2003;100:8520-5. doi:10.1073/pnas.1332574100.
Liu J, Lee HJ, Weitz AJ, Fang Z, Lin P, Choy M, Fisher R, Pinskiy V, Tolpygo A, Mitra P, Schiff N, Lee JH. Frequency-selective control of cortical and subcortical networks by central thalamus. Elife. 2015 Dec 10;4:e09215. doi:10.7554/eLife.09215