Neural plasticity lessons from disorders of consciousness

consciousness; unresponsive wakefulness syndrome; vegetative state; recovery; neural plasticity; minimally conscious state; functional neuroimaging; deep brain stimulation

Abstract :

[en] Communication and intentional behavior are supported by the brain?s integrity at a structural and a functional level. When widespread loss of cerebral connectivity is brought about as a result of a severe brain injury, in many cases patients are not capable of conscious interactive behavior and are said to suffer from disorders of consciousness (e.g., coma, vegetative state /unresponsive wakefulness syndrome, minimally conscious states). This lesion paradigm has offered not only clinical insights, as how to improve diagnosis, prognosis and treatment, but also put forward scientific opportunities to study the brain?s plastic abilities. We here review interventional and observational studies performed in severely brain-injured patients with regards to recovery of consciousness. The study of the recovered conscious brain (spontaneous and/or after surgical or pharmacologic interventions), suggests a link between some specific brain areas and the capacity of the brain to sustain conscious experience, challenging at the same time the notion of fixed temporal boundaries in rehabilitative processes. Altered functional connectivity, cerebral structural reorganization as well as behavioral amelioration after invasive treatments will be discussed as the main indices for plasticity in these challenging patients. The study of patients with chronic disorders of consciousness may, thus, provide further insights not only at a clinical level (i.e., medical management and rehabilitation) but also from a scientific-theoretical perspective (i.e., the brain?s plastic abilities and the pursuit of the neural correlate of consciousness).

Disciplines :

Neurology

Author, co-author :

Demertzi, Athina ; Université de Liège - ULiège > Centre de recherches du cyclotron

Schnakers, Caroline ; Université de Liège - ULiège > Centre de recherches du cyclotron

Soddu, Andrea ; Université de Liège - ULiège > Centre de recherches du cyclotron

Bruno, Marie-Aurélie ; Université de Liège - ULiège > Centre de recherches du cyclotron

Gosseries, Olivia ; Université de Liège - ULiège > Centre de recherches du cyclotron

Vanhaudenhuyse, Audrey ; Université de Liège - ULiège > Centre de recherches du cyclotron

Laureys, Steven ; Université de Liège - ULiège > Centre de recherches du cyclotron

Language :

English

Title :

Neural plasticity lessons from disorders of consciousness

Publication date :

February 2011

Journal title :

Frontiers in Psychology

eISSN :

1664-1078

Publisher :

Frontiers Media S.A., Switzerland

Volume :

Pages :

1-7

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 28 June 2011

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Bibliography

Adams, J. H., Graham, D. I., and Jennett, B. (2000). The neuropathology of the vegetative state after an acute brain insult. Brain 123(Pt 7), 1327-1338.
Arfanakis, K., Haughton, V. M., Carew, J. D., Rogers, B. P., Dempsey, R. J., and Meyerand, M. E. (2002). Diffusion tensor MR imaging in diffuse axonal injury. Am. J. Neuroradiol. 23, 794-802.
Baars, B. J., Ramsoy, T. Z., and Laureys, S. (2003). Brain, conscious experience and the observing self. Trends Neurosci. 26, 671-675.
Boly, M., Balteau, E., Schnakers, C., Degueldre, C., Moonen, G., Luxen, A., Phillips, C., Peigneux, P., Maquet, P., and Laureys, S. (2007). Baseline brain activity fluctuations predict somatosensory perception in humans. Proc. Natl. Acad. Sci. U.S.A. 104, 12187-12192.
Boly, M., Faymonville, M. E., Peigneux, P., Lambermont, B., Damas, P., Del Fiore, G., Degueldre, C., Franck, G., Luxen, A., Lamy, M., Moonen, G., Maquet, P., and Laureys, S. (2004). Auditory processing in severely brain injured patients: differences between the minimally conscious state and the persistent vegetative state. Arch. Neurol. 61, 233-238.
Boly, M., Faymonville, M. E., Schnakers, C., Peigneux, P., Lambermont, B., Phillips, C., Lancellotti, P., Luxen, A., Lamy, M., Moonen, G., Maquet, P., and Laureys, S. (2008a). Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol. 7, 1013-1020.
Boly, M., Phillips, C., Tshibanda, L., Vanhaudenhuyse, A., Schabus, M., Dang-Vu, T. T., Moonen, G., Hustinx, R., Maquet, P., and Laureys, S. (2008b). Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function? Ann. N.Y. Acad. Sci. 1129, 119-129.
Boly, M., Tshibanda, L., Vanhaudenhuyse, A., Noirhomme, Q., Schnakers, C., Ledoux, D., Boveroux, P., Garweg, C., Lambermont, B., Phillips, C., Luxen, A., Moonen, G., Bassetti, C., Maquet, P., and Laureys, S. (2009). Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum. Brain Mapp. 30, 2393-2400.
Boveroux, P., Vanhaudenhuyse, A., Bruno, M. A., Noirhomme, Q., Lauwick, S., Luxen, A., Degueldre, C., Perlbarg, V., Plenevaux, A., Schnakers, C., Phillips, C., Brichant, J. F., Bohnomme, V., Maquet, P., Greicius, M. D., Laureys, S., and Boly, M. (2010). Breakdown of within- and between-network resting state functional magnetic resonance imaging connectivity during propofol-induced loss of consciousness. Anesthesiology 113, 1038-1053.
Bruno, M. A., Soddu, A., Demertzi, A., Laureys, S., Gosseries, O., Schnackers, C., Boly, M., Noirhomme, Q., Thonnard, M., Chatelle, C., and Vanhaudenhuyse, A. (2010). Disorders of consciousness: moving from passive to resting state and active paradigms. Cogn. Neurosci. 1, 193-203.
Buckner, R. L., Andrews-Hanna, J. R., and Schacter, D. L. (2008). The brain's default network: anatomy, function, and relevance to disease. Ann. N.Y. Acad. Sci. 1124, 1-38.
Carpentier, A., Galanaud, D., Puybasset, L., Muller, J. C., Lescot, T., Boch, A. L., Riedl, V., Cornu, P., Coriat, P., Dormont, D., and van Effenterre, R. (2006). Early morphologic and spectroscopic magnetic resonance in severe traumatic brain injuries can detect " invisible brain stem damage" and predict " vegetative states". J. Neurotrauma 23, 674-685.
Cohadon, F., and Richer, E. (1993). [Deep cerebral stimulation in patients with post-traumatic vegetative state. 25 cases]. Neurochirurgie 39, 281-292.
Coleman, M. R., Rodd, J. M., Davis, M. H., Johnsrude, I. S., Menon, D. K., Pickard, J. D., and Owen, A. M. (2007). Do vegetative patients retain aspects of language comprehension? Evidence from fMRI. Brain 130, 2494-2507.
Dehaene, S., Changeux, J. P., Naccache, L., Sackur, J., and Sergent, C. (2006). Conscious, preconscious, and subliminal processing: a testable taxonomy. Trends Cogn. Sci. 10, 204-211.
Demertzi, A., Soddu, A., Faymonville, M. E., Bahri, M. A., Gosseries, O., Vanhaudenhuyse, A., Phillips, C., Maquet, P., Noirhomme, Q., Luxen, A., and Laureys, S. (in press). Hypnotic modulation of resting state fMRI default mode and extrinsic network connectivity. Prog. Brain Res.
Demertzi, A., Vanhaudenhuyse, A., Bruno, M. A., Schnakers, C., Boly, M., Boveroux, P., Maquet, P., Moonen, G., and Laureys, S. (2008). Is there anybody in there? Detecting awareness in disorders of consciousness. Expert Rev. Neurother. 8, 1719-1730.
Di, H. B., Yu, S. M., Weng, X. C., Laureys, S., Yu, D., Li, J. Q., Qin, P. M., Zhu, Y. H., Zhang, S. Z., and Chen, Y. Z. (2007). Cerebral response to patient's own name in the vegetative and minimally conscious states. Neurology 68, 895-899.
Estraneo, A., Moretta, P., Loreto, V., Lanzillo, B., Santoro, L., and Trojano, L. (2010). Late recovery after traumatic, anoxic, or hemorrhagic longlasting vegetative state. Neurology 75, 239-245.
Fins, J. J., Illes, J., Bernat, J. L., Hirsch, J., Laureys, S., and Murphy, E. (2008). Neuroimaging and disorders of consciousness: envisioning an ethical research agenda. Am. J. Bioeth. 8, 3-12.
Friston, K. (2002). Beyond phrenology: what can neuroimaging tell us about distributed circuitry? Annu. Rev. Neurosci. 25, 221-250.
Giacino, J. T., Ashwal, S., Childs, N., Cranford, R., Jennett, B., Katz, D. I., Kelly, J. P., Rosenberg, J. H., Whyte, J., Zafonte, R. D., and Zasler, N. D. (2002). The minimally conscious state: definition and diagnostic criteria. Neurology 58, 349-353.
Gould, E., Reeves, A. J., Graziano, M. S., and Gross, C. G. (1999). Neurogenesis in the neocortex of adult primates. Science 286, 548-552.
Jennett, B., and Plum, F. (1972). Persistent vegetative state after brain damage. A syndrome in search of a name. Lancet 1, 734-737.
Laureys, S. (2005). The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn. Sci. 9, 556-559.
Laureys, S., Celesia, G. G., Cohadon, F., Lavrijsen, J., Leon-Carrion, J., Sannita, W. G., Sazbon, L., Schmutzhard, E., von Wild, K. R., Zeman, A., and Dolce, G. (2010). Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med. 8, 68. doi: 10.1186/1741-7015-8-68
Laureys, S., Faymonville, M. E., Degueldre, C., Fiore, G. D., Damas, P., Lambermont, B., Janssens, N., Aerts, J., Franck, G., Luxen, A., Moonen, G., Lamy, M., and Maquet, P. (2000a). Auditory processing in the vegetative state. Brain 123, 1589-1601.
Laureys, S., Faymonville, M. E., Luxen, A., Lamy, M., Franck, G., and Maquet, P. (2000b). Restoration of thalamocortical connectivity after recovery from persistent vegetative state. Lancet 355, 1790-1791.
Laureys, S., Faymonville, M. E., Peigneux, P., Damas, P., Lambermont, B., Del Fiore, G., Degueldre, C., Aerts, J., Luxen, A., Franck, G., Lamy, M., Moonen, G., and Maquet, P. (2002). Cortical processing of noxious somatosensory stimuli in the persistent vegetative state. Neuroimage 17, 732-741.
Laureys, S., Boly, M., and Maquet, P. (2006a). Tracking the recovery of consciousness from coma. J. Clin. Invest. 116, 1823-1825.
Laureys, S., Giacino, J. T., Schiff, N. D., Schabus, M., and Owen, A. M. (2006b). How should functional imaging of patients with disorders of consciousness contribute to their clinical rehabilitation needs? Curr. Opin. Neurol. 19, 520-527.
Laureys, S., Goldman, S., Phillips, C., Van Bogaert, P., Aerts, J., Luxen, A., Franck, G., and Maquet, P. (1999). Impaired effective cortical connectivity in vegetative state: preliminary investigation using PET. Neuroimage 9, 377-382.
Laureys, S., Owen, A. M., and Schiff, N. D. (2004a). Brain function in coma, vegetative state, and related disorders. Lancet Neurol. 3, 537-546.
Laureys, S., Perrin, F., Faymonville, M. E., Schnakers, C., Boly, M., Bartsch, V., Majerus, S., Moonen, G., and Maquet, P. (2004b). Cerebral processing in the minimally conscious state. Neurology 63, 916-918.
Lescot, T., Galanaud, D., and Puybasset, L. (2009). Exploring altered consciousness states by magnetic resonance imaging in brain injury. Ann. N.Y. Acad. Sci. 1157, 71-80.
Lombardi, F., Taricco, M., De Tanti, A., Telaro, E., and Liberati, A. (2002). Sensory stimulation of brain-injured individuals in coma or vegetative state: results of a Cochrane systematic review. Clin. Rehabil. 16, 464-472.
Majerus, S., Gill-Thwaites, H., Andrews, K., and Laureys, S. (2005). Behavioral evaluation of consciousness in severe brain damage. Prog. Brain Res. 150, 397-413.
Mason, M. F., Norton, M. I., Van Horn, J. D., Wegner, D. M., Grafton, S. T., and Macrae, C. N. (2007). Wandering minds: the default network and stimulus-independent thought. Science 315, 393-395.
McGeown, W. J., Mazzoni, G., Venneri, A., and Kirsch, I. (2009). Hypnotic induction decreases anterior default mode activity. Conscious Cogn. 18, 848-555.
Monti, M. M., Laureys, S., and Owen, A. M. (2010a). The vegetative state. BMJ 341, c3765.
Monti, M. M., Vanhaudenhuyse, A., Coleman, M. R., Boly, M., Pickard, J. D., Tshibanda, L., Owen, A., and Laureys, S. (2010b). Willful modulation of brain activity in disorders of consciousness. N. Engl. J. Med. 362, 579-589.
Oh, H., and Seo, W. (2003). Sensory stimulation programme to improve recovery in comatose patients. J. Clin. Nurs. 12, 394-404.
Owen, A. M., Coleman, M. R., Boly, M., Davis, M. H., Laureys, S., and Pickard, J. D. (2006). Detecting awareness in the vegetative state. Science 313, 1402.
Passler, M. A., and Riggs, R. V. (2001). Positive outcomes in traumatic brain injury-vegetative state: patients treated with bromocriptine. Arch. Phys. Med. Rehabil. 82, 311-315.
Pistoia, F., Mura, E., Govoni, S., Fini, M., and Sara, M. (2010). Awakenings and awareness recovery in disorders of consciousness: is there a role for drugs? CNS Drugs 24, 625-638.
Sawyer, E., Mauro, L. S., and Ohlinger, M. J. (2008). Amantadine enhancement of arousal and cognition after traumatic brain injury. Ann. Pharmacother. 42, 247-252.
Schiff, N. D. (2010). Recovery of consciousness after brain injury: a mesocircuit hypothesis. Trends Neurosci. 33, 1-9.
Schiff, N. D., and Fins, J. J. (2007). Deep brain stimulation and cognition: moving from animal to patient. Curr. Opin. Neurol. 20, 638-642.
Schiff, N. D., Giacino, J. T., Kalmar, K., Victor, J. D., Baker, K., Gerber, M., Fritz, B., Eisenberg, B., O'Connor, J., Kobylarz, E. J., Farris, S., Machado, A., McCagg, C., Plum, F., Fins, J. J., and Rezai, A. R. (2007). Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448, 600-603.
Schiff, N. D., Ribary, U., Moreno, D. R., Beattie, B., Kronberg, E., Blasberg, R., Giacino, J. T., McCagg, C., Fins, J. J., Llinas, R., and Plum, F. (2002). Residual cerebral activity and behavioural fragments can remain in the persistently vegetative brain. Brain 125, 1210-1234.
Schnakers, C., Hustinx, R., Vandewalle, G., Majerus, S., Moonen, G., Boly, M., Vanhaudenhuyse, A., and Laureys, S. (2008). Measuring the effect of amantadine in chronic anoxic minimally conscious state. J. Neurol. Neurosurg. Psychiatry 79, 225-227.
Shiel, A., Burn, J. P., Henry, D., Clark, J., Wilson, B. A., Burnett, M. E., and McLellan, D. L. (2001). The effects of increased rehabilitation therapy after brain injury: results of a prospective controlled trial. Clin. Rehabil. 15, 501-514.
Soddu, A., Boly, M., Nir, Y., Noirhomme, Q., Vanhaudenhuyse, A., Demertzi, A., Arzi, A., Ovadia, S., Stanziano, M., Papa, M., Laureys, S., and Malach, R. (2009). Reaching across the abyss: recent advances in functional magnetic resonance imaging and their potential relevance to disorders of consciousness. Prog. Brain Res. 177, 261-274.
Soddu, A., Vanhaudenhuyse, A., Bahri, M., A., Bruno, M. A., Boly, M., Demertzi, A., Tshibanda, J., Phillips, C., Stanziano, M., Ovadia-Caro, S., Nir, Y., Maquet, P., Papa, M., Malach, R., Laureys, S., and Noirhomme, Q. (in press). Identifying the default mode component in spatial ICA of patients with disorders of consciousness. Hum. Brain Mapp.
Taira, T., and Hori, T. (2007). Intrathecal baclofen in the treatment of poststroke central pain, dystonia, and persistent vegetative state. Acta Neurochir. Suppl. 97, 227-229.
The Multi-Society Task Force on PVS. (1994). Medical aspects of the persistent vegetative state (2). N. Engl. J. Med. 330, 1572-1579.
Tolle, P., and Reimer, M. (2003). Do we need stimulation programs as a part of nursing care for patients in " persistent vegetative state" ? A conceptual analysis. Axone 25, 20-26.
Tononi, G., and Laureys, S. (2009). " The neurology of consciousness: an overview," in The Neurology of Consciousness: Cognitive Neuroscience and Neuropathology, eds S. Laureys and G. Tononi (Oxford, UK: Academic Press), 375-412.
Tshibanda, L., Vanhaudenhuyse, A., Boly, M., Soddu, A., Bruno, M. A., Moonen, G., Laureys, S., and Noirhomme, Q. (2010). Neuroimaging after coma. Neuroradiology 52, 15-24.
Tshibanda, L., Vanhaudenhuyse, A., Galanaud, D., Boly, M., Laureys, S., and Puybasset, L. (2009). Magnetic resonance spectroscopy and diffusion tensor imaging in coma survivors: promises and pitfalls. Prog. Brain Res. 177, 215-229.
Vanhaudenhuyse, A., Demertzi, A., Schabus, M., Noirhomme, Q., Bredart, S., Boly, M., Phillips, C., Soddu, A., Luxen, A., Moonen, G., and Laureys, S. (2011). Two distinct neuronal networks mediate the awareness of environment and of self. J. Cogn. Neurosci. 23, 570-578.
Vanhaudenhuyse, A., Noirhomme, Q., Tshibanda, L. J., Bruno, M. A., Boveroux, P., Schnakers, C., Soddu, A., Perlbarg, V., Ledoux, D., Brichant, J. F., Moonen, G., Maquet, P., Greicius, M. D., Laureys, S., and Boly, M. (2009). Default network connectivity reflects the level of consciousness in non-communicative braindamaged patients. Brain 133, 161-171.
Vanhaudenhuyse, A., Schnakers, C., Bredart, S., and Laureys, S. (2008). Assessment of visual pursuit in postcomatose states: use a mirror. J. Neurol. Neurosurg. Psychiatry 79, 223.
Vogt, B. A., and Laureys, S. (2005). Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. Prog. Brain Res. 150, 205-217.
Voss, H. U., Uluc, A. M., Dyke, J. P., Watts, R., Kobylarz, E. J., McCandliss, B. D., Heier, L. A., Beattie, B. J., Hamacher, K. A., Vallabhajosula, S., Goldsmith, S.J., Ballon, D., Giacino, J.T., and Schiff, N. D. (2006). Possible axonal regrowth in late recovery from the minimally conscious state. J. Clin. Invest. 116, 2005-2011.
Whyte, J., Katz, D., Long, D., DiPasquale, M. C., Polansky, M., Kalmar, K., Giacino, J. T., Childs, N., Mercer, W., Novak, P., Maurer, P., and Eifert, B. (2005). Predictors of outcome in prolonged posttraumatic disorders of consciousness and assessment of medication effects: a multicenter study. Arch. Phys. Med. Rehabil. 86, 453-462.
Yamamoto, T., Katayama, Y., Oshima, H., Fukaya, C., Kawamata, T., and Tsubokawa, T. (2001). Deep brain stimulation therapy for a persistent vegetative state. Acta Neurochir. Suppl. 79, 79-82.