Disorders of consciousness; Magnetic resonance imaging; Minimally conscious state; Positron emission tomography; Transcranial direct current stimulation; Treatment; Voxel-based morphometry
Résumé :
[en] BACKGROUND: Transcranial direct current stimulation (tDCS) was recently shown to promote recovery of voluntary signs of consciousness in some patients in minimally conscious state (MCS). However, it remains unclear why clinical improvement is only observed in a subgroup of patients. OBJECTIVES: In this retrospective study, we investigated the relationship between tDCS responsiveness and neuroimaging data from MCS patients. METHODS: Structural Magnetic Resonance Imaging (MRI), Fluorodeoxyglucose Positron emission tomography (FDG-PET) and clinical electroencephalography (EEG) were acquired in 21 sub-acute and chronic MCS patients (8 tDCS responders) who subsequently (<48 h) received left dorsolateral prefrontal (DLPF) tDCS in a double-blind randomized cross-over trial. The behavioral data have been published elsewhere (Thibaut et al., Neurology, 2014). RESULTS: Grey matter atrophy was observed in non-responders as compared with responders in the left DLPF cortex, the medial-prefrontal cortex, the cingulate cortex, the hippocampi, part of the rolandic regions, and the left thalamus. FDG-PET showed hypometabolism in non-responders as compared with responders in the left DLPF cortex, the medial-prefrontal cortex, the precuneus, and the thalamus. EEG did not show any difference between the two groups. CONCLUSION: Our findings suggest that the transient increase of signs of consciousness following left DLPF tDCS in patients in MCS require grey matter preservation and residual metabolic activity in cortical and subcortical brain areas known to be involved in attention and working memory. These results further underline the critical role of long-range cortico-thalamic connections in consciousness recovery, providing important information for guidelines on the use of tDCS in disorders of consciousness.
M.A. Nitsche, and W. Paulus Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation J Physiol 527 Pt 3 2000 633 639
M.A. Nitsche, A. Seeber, K. Frommann, and et al. Modulating parameters of excitability during and after transcranial direct current stimulation of the human motor cortex J Physiol 568 Pt 1 2005 291 303
D. Liebetanz, M.A. Nitsche, F. Tergau, and W. Paulus Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability Brain 125 Pt 10 2002 2238 2247
C.J. Stagg, and M.A. Nitsche Physiological basis of transcranial direct current stimulation Neuroscientist 17 1 2011 37 53
U.G. Kalu, C.E. Sexton, C.K. Loo, and K.P. Ebmeier Transcranial direct current stimulation in the treatment of major depression: A meta-analysis Psychol Med 2012 1 10
V. Mylius, J.J. Borckardt, and J.P. Lefaucheur Noninvasive cortical modulation of experimental pain Pain 153 7 2012 1350 1363
B. Langguth, and D. De Ridder Tinnitus: therapeutic use of superficial brain stimulation Handb Clin Neurol 116 2013 441 467
M. Sandrini, and L.G. Cohen Noninvasive brain stimulation in neurorehabilitation Handb Clin Neurol 116 2013 499 524
P.S. Boggio, R. Ferrucci, S.P. Rigonatti, and et al. Effects of transcranial direct current stimulation on working memory in patients with Parkinson's disease J Neurol Sci 249 1 2006 31 38
E.K. Kang, M.J. Baek, S. Kim, and N.J. Paik Non-invasive cortical stimulation improves post-stroke attention decline Restor Neurol Neurosci 27 6 2009 645 650
R. Ferrucci, F. Mameli, I. Guidi, and et al. Transcranial direct current stimulation improves recognition memory in Alzheimer disease Neurology 71 7 2008 493 498
A. Thibaut, M.A. Bruno, D. Ledoux, A. Demertzi, and S. Laureys tDCS in patients with disorders of consciousness: sham-controlled randomised double blind study Neurology 82 13 2014 1112 1118
M.A. Nitsche, L.G. Cohen, E.M. Wassermann, and et al. Transcranial direct current stimulation: state of the art 2008 Brain Stimul 1 3 2008 206 223
M.A. Nitsche, and W. Paulus Transcranial direct current stimulation-update 2011 Restor Neurol Neurosci 29 6 2011 463 492
J.J. Song, S. Vanneste, P. Van de Heyning, and D. De Ridder Transcranial direct current stimulation in tinnitus patients: A systemic review and meta-analysis ScientificWorldJournal 2012 2012 427941
R. Ferrucci, M. Vergari, F. Cogiamanian, and et al. Transcranial direct current stimulation (tDCS) for fatigue in multiple sclerosis NeuroRehabilitation 34 1 2014 121 127
G.S. Goncalves, I.C. Borges, B.T. Goes, and et al. Effects of tDCS induced motor cortex modulation on pain in HTLV-1: A blind randomized clinical trial Clin J Pain 30 9 2013 809 815
J.C. Horvath, J.D. Forte, and O. Carter Quantitative review finds no evidence of cognitive effects in healthy populations from single-session transcranial direct current stimulation (tDCS) Brain Stimul 8 3 2015 May-June 2015, 535-550
A.R. Price, and R.H. Hamilton A re-evaluation of the cognitive effects from single-session transcranial direct current stimulation Brain Stimul 2015
J. Reis, H.M. Schambra, L.G. Cohen, and et al. Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation Proc Natl Acad Sci U S A 106 5 2009 1590 1595
J. Whyte Disorders of consciousness: the changing landscape of treatment Neurology 82 13 2014 1106 1107
J.T. Giacino, S. Ashwal, N. Childs, and et al. The minimally conscious state: definition and diagnostic criteria Neurology 58 3 2002 349 353
M.A. Nitsche, D. Liebetanz, N. Lang, A. Antal, F. Tergau, and W. Paulus Safety criteria for transcranial direct current stimulation (tDCS) in humans Clin Neurophysiol 114 11 2003 2220 2222 Author reply 2222-2223
J. Stender, O. Gosseries, M.A. Bruno, and et al. Diagnostic precision of multimodal neuroimaging methods in disorders of consciousness: A clinical validation study Lancet 384 9942 2014 514 522
M.A. Nitsche, and W. Paulus Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans Neurology 57 2001 1899 1901
U. Herwig, P. Satrapi, and C. Schonfeldt-Lecuona Using the international 10-20 EEG system for positioning of transcranial magnetic stimulation Brain Topogr 16 2 2003 95 99
J.T. Giacino The vegetative and minimally conscious states: consensus-based criteria for establishing diagnosis and prognosis NeuroRehabilitation 19 4 2004 293 298
R. Lehembre, M.A. Bruno, A. Vanhaudenhuyse, and et al. Resting-state EEG study of comatose patients: A connectivity and frequency analysis to find differences between vegetative and minimally conscious states Funct Neurol 27 1 2012 41 47
J. Ashburner A fast diffeomorphic image registration algorithm Neuroimage 38 1 2007 95 113
R. Takahashi, K. Ishii, N. Miyamoto, and et al. Measurement of gray and white matter atrophy in dementia with Lewy bodies using diffeomorphic anatomic registration through exponentiated lie algebra: A comparison with conventional voxel-based morphometry AJNR Am J Neuroradiol 31 10 2010 1873 1878
J.E. Peelle, R. Cusack, and R.N. Henson Adjusting for global effects in voxel-based morphometry: gray matter decline in normal aging Neuroimage 60 2 2012 1503 1516
C. Di Perri, S. Bastianello, A.J. Bartsch, and et al. Limbic hyperconnectivity in the vegetative state Neurology 81 16 2013 1417 1424
S. Laureys, M.E. Faymonville, G. Moonen, A. Luxen, and P. Maquet PET scanning and neuronal loss in acute vegetative state Lancet 355 9217 2000 1825 1826 Author reply 1827
M. Quarantelli, K. Berkouk, A. Prinster, and et al. Integrated software for the analysis of brain PET/SPECT studies with partial-volume-effect correction J Nucl Med 45 2 2004 192 201
C.L. Phillips, M.A. Bruno, P. Maquet, and et al. "Relevance vector machine" consciousness classifier applied to cerebral metabolism of vegetative and locked-in patients Neuroimage 56 2 2011 797 808
A. Thibaut, M.A. Bruno, C. Chatelle, and et al. Metabolic activity in external and internal awareness networks in severely brain-damaged patients J Rehabil Med 44 6 2012 487 494
M.A. Bruno, S. Majerus, M. Boly, and et al. Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients J Neurol 259 6 2012 1087 1098
G. Schlaug, V. Renga, and D. Nair Transcranial direct current stimulation in stroke recovery Arch Neurol 65 12 2008 1571 1576
O. Gosseries, S. Sarasso, S. Casarotto, and et al. On the cerebral origin of EEG responses to TMS: insights from severe cortical lesions Brain Stimul 8 1 2015 142 149
M. D'Esposito, D. Ballard, G.K. Aguirre, and E. Zarahn Human prefrontal cortex is not specific for working memory: A functional MRI study Neuroimage 8 3 1998 274 282
M. D'Esposito, J.A. Detre, D.C. Alsop, R.K. Shin, S. Atlas, and M. Grossman The neural basis of the central executive system of working memory Nature 378 6554 1995 279 281
O. Devinsky, and M. D'Esposito Neurology of cognitive and behavioural disorders 2004 Oxford University Press Oxford, New York
M.D. Lieberman Social cognitive neuroscience: A review of core processes Annu Rev Psychol 58 2007 259 289
S. Laureys, S. Goldman, C. Phillips, and et al. Impaired effective cortical connectivity in vegetative state: preliminary investigation using PET Neuroimage 9 4 1999 377 382
S. Laureys Functional neuroimaging in the vegetative state NeuroRehabilitation 19 4 2004 335 341
A. Vanhaudenhuyse, Q. Noirhomme, L.J. Tshibanda, and et al. Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients Brain 133 Pt 1 2010 161 171
N.D. Schiff Recovery of consciousness after brain injury: A mesocircuit hypothesis Trends Neurosci 33 1 2010 1 9
E.A. Fridman, B.J. Beattie, A. Broft, S. Laureys, and N.D. Schiff Regional cerebral metabolic patterns demonstrate the role of anterior forebrain mesocircuit dysfunction in the severely injured brain Proc Natl Acad Sci U S A 111 17 2014 6473 6478
D. Fernandez-Espejo, A. Soddu, D. Cruse, and et al. A role for the default mode network in the bases of disorders of consciousness Ann Neurol 72 3 2012 335 343
S. Laureys, M. Boly, and P. Maquet Tracking the recovery of consciousness from coma J Clin Invest 116 7 2006 1823 1825
A. Vanhaudenhuyse, A. Demertzi, M. Schabus, and et al. Two distinct neuronal networks mediate the awareness of environment and of self J Cogn Neurosci 23 3 2011 570 578
N. Lang, H.R. Siebner, N.S. Ward, and et al. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain? Eur J Neurosci 22 2 2005 495 504
C.J. Stagg, V. Bachtiar, J. O'Shea, and et al. Cortical activation changes underlying stimulation-induced behavioural gains in chronic stroke Brain 135 Pt 1 2012 276 284
D. Keeser, T. Meindl, J. Bor, and et al. Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI J Neurosci 31 43 2011 15284 15293
B. Clemens, S. Jung, G. Mingoia, D. Weyer, F. Domahs, and K. Willmes Influence of anodal transcranial direct current stimulation (tDCS) over the right angular gyrus on brain activity during rest PLoS One 9 4 2014 e95984
C. Pena-Gomez, R. Sala-Lonch, C. Junque, and et al. Modulation of large-scale brain networks by transcranial direct current stimulation evidenced by resting-state functional MRI Brain Stimul 5 3 2012 252 263
S. Laureys, M.E. Faymonville, A. Luxen, M. Lamy, G. Franck, and P. Maquet Restoration of thalamocortical connectivity after recovery from persistent vegetative state Lancet 355 9217 2000 1790 1791
N.D. Schiff, J.T. Giacino, K. Kalmar, and et al. Behavioural improvements with thalamic stimulation after severe traumatic brain injury Nature 448 7153 2007 600 603
S. Frisch, J. Dukart, B. Vogt, and et al. Dissociating memory networks in early Alzheimer's disease and frontotemporal lobar degeneration - a combined study of hypometabolism and atrophy PLoS One 8 2 2013 e55251
M. Schecklmann, A. Lehner, T.B. Poeppl, and et al. Cluster analysis for identifying sub-types of tinnitus: A positron emission tomography and voxel-based morphometry study Brain Res 1485 2012 3 9
K. Shima, I. Matsunari, M. Samuraki, and et al. Posterior cingulate atrophy and metabolic decline in early stage Alzheimer's disease Neurobiol Aging 33 9 2012 2006 2017
Y.G. Weber, R. Roebling, J. Kassubek, and et al. Comparative analysis of brain structure, metabolism, and cognition in myotonic dystrophy 1 and 2 Neurology 74 14 2010 1108 1117
T. Kanda, K. Ishii, T. Uemura, and et al. Comparison of grey matter and metabolic reductions in frontotemporal dementia using FDG-PET and voxel-based morphometric MR studies Eur J Nucl Med Mol Imaging 35 12 2008 2227 2234
R. Gonzalez-Redondo, D. Garcia-Garcia, P. Clavero, and et al. Grey matter hypometabolism and atrophy in Parkinson's disease with cognitive impairment: A two-step process Brain 137 Pt 8 2014 2356 2367
J.H. Adams, D.I. Graham, and B. Jennett The neuropathology of the vegetative state after an acute brain insult Brain 123 Pt 7 2000 1327 1338
L. Tshibanda, A. Vanhaudenhuyse, M. Boly, and et al. Neuroimaging after coma Neuroradiology 52 1 2010 15 24
M. Song, Y. Shin, and K. Yun Beta-frequency EEG activity increased during transcranial direct current stimulation Neuroreport 25 18 2014 1433 1436
D. Keeser, F. Padberg, E. Reisinger, and et al. Prefrontal direct current stimulation modulates resting EEG and event-related potentials in healthy subjects: A standardized low resolution tomography (sLORETA) study Neuroimage 55 2 2011 644 657
F. Ulam, C. Shelton, L. Richards, and et al. Cumulative effects of transcranial direct current stimulation on EEG oscillations and attention/working memory during subacute neurorehabilitation of traumatic brain injury Clin Neurophysiol 126 3 2014 486 496
