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Progression from Vegetative to Minimally Conscious State Is Associated with Changes in Brain Neural Response to Passive Tasks: A Longitudinal Single-Case Functional MRI Study

Published online by Cambridge University Press:  06 June 2016

Francesco Tomaiuolo ,
Luca Cecchetti ,
Raechelle M. Gibson ,
Fiammetta Logi ,
Adrian M. Owen ,
Franco Malasoma ,
Sabino Cozza ,
Pietro Pietrini  and
Emiliano Ricciardi
Francesco Tomaiuolo
Affiliation:
Unità Gravi Cerebrolesioni Acquisite, Auxilium Vitae Volterra, Pisa, Italy Clinical Psychology Branch, Pisa University Hospital, Pisa, Italy Laboratory of Clinical Biochemistry and Molecular Biology, Department of Surgical, Medical and Molecular Pathology and Critical Care, University of Pisa, Pisa, Italy
Luca Cecchetti*
Affiliation:
Unità Gravi Cerebrolesioni Acquisite, Auxilium Vitae Volterra, Pisa, Italy Clinical Psychology Branch, Pisa University Hospital, Pisa, Italy Laboratory of Clinical Biochemistry and Molecular Biology, Department of Surgical, Medical and Molecular Pathology and Critical Care, University of Pisa, Pisa, Italy
Raechelle M. Gibson
Affiliation:
The Brain and Mind Institute, Department of Psychology, University of Western Ontario, London, N6A 5B7, Canada
Fiammetta Logi
Affiliation:
Unità Gravi Cerebrolesioni Acquisite, Auxilium Vitae Volterra, Pisa, Italy
Adrian M. Owen
Affiliation:
The Brain and Mind Institute, Department of Psychology, University of Western Ontario, London, N6A 5B7, Canada
Franco Malasoma
Affiliation:
U.O. Radiologia, ASL5 Volterra, Pisa, Italy
Sabino Cozza
Affiliation:
U.O. Radiologia, ASL5 Volterra, Pisa, Italy
Pietro Pietrini
Affiliation:
Clinical Psychology Branch, Pisa University Hospital, Pisa, Italy Laboratory of Clinical Biochemistry and Molecular Biology, Department of Surgical, Medical and Molecular Pathology and Critical Care, University of Pisa, Pisa, Italy IMT School for Advanced Studies Lucca, Lucca, Italy
Emiliano Ricciardi
Affiliation:
Laboratory of Clinical Biochemistry and Molecular Biology, Department of Surgical, Medical and Molecular Pathology and Critical Care, University of Pisa, Pisa, Italy
*
Correspondence and reprint requests to: Luca Cecchetti, Via Roma, 67 - Building 43, 56100 Pisa, Italy. E-mail: [email protected]
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Abstract

Objectives: Functional magnetic resonance imaging (fMRI) may be adopted as a complementary tool for bedside observation in the disorders of consciousness (DOC). However, the diagnostic value of this technique is still debated because of the lack of accuracy in determining levels of consciousness within a single patient. Recently, Giacino and colleagues (2014) hypothesized that a longitudinal fMRI evaluation may provide a more informative assessment in the detection of residual awareness. The aim of this study was to measure the correspondence between clinically defined level of awareness and neural responses within a single DOC patient. Methods: We used a follow-up fMRI design in combination with a passive speech-processing task. Patient’s consciousness was measured through time by using the Coma Recovery Scale. Results: The patient progressed from a vegetative state (VS) to a minimally conscious state (MCS). Patient’s task-related neural responses mirrored the clinical change from a VS to an MCS. Specifically, while in an MCS, but not a VS, the patient showed a selective recruitment of the left angular gyrus when he listened to a native speech narrative, as compared to the reverse presentation of the same stimulus. Furthermore, the patient showed an increased response in the language-related brain network and a greater deactivation in the default mode network following his progression to an MCS. Conclusions: Our findings indicate that longitudinal assessment of brain responses to passive stimuli can contribute to the definition of the clinical status in individual patients with DOC and represents an adequate counterpart of the bedside assessment during the diagnostic decision-making process. (JINS, 2016, 22, 620–630)

Keywords

Disorders of consciousnessfMRIVegetative stateMinimally conscious stateLanguage processingLongitudinal design
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 22 , Issue 6 , July 2016 , pp. 620 - 630
Copyright
Copyright © The International Neuropsychological Society 2016 

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References

Bekinschtein, T., Leiguarda, R., Armony, J., Owen, A., Carpintiero, S., Niklison, J., & Manes, F. (2004). Emotion processing in the minimally conscious state. Journal of Neurology, Neurosurgery, and Psychiatry, 75(5), 788.Google Scholar
Bekinschtein, T., Tiberti, C., Niklison, J., Tamashiro, M., Ron, M., Carpintiero, S., & Manes, F. (2005). Assessing level of consciousness and cognitive changes from vegetative state to full recovery. Neuropsychological Rehabilitation, 15(3-4), 307–322. doi:10.1080/09602010443000443 Google Scholar
Bernat, J.L. (2006). Chronic disorders of consciousness. Lancet, 367(9517), 1181–1192. doi:10.1016/S0140-6736(06)68508-5 Google Scholar
Boly, M., Faymonville, M.E., Schnakers, C., Peigneux, P., Lambermont, B., Phillips, C., & Laureys, S. (2008). Perception of pain in the minimally conscious state with PET activation: An observational study. Lancet Neurology, 7(11), 1013–1020. doi:10.1016/S1474-4422(08)70219-9 CrossRefGoogle ScholarPubMed
Boly, M., Tshibanda, L., Vanhaudenhuyse, A., Noirhomme, Q., Schnakers, C., Ledoux, D., & Laureys, S. (2009). Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Human Brain Mapping, 30(8), 2393–2400. doi:10.1002/hbm.20672 Google Scholar
Bonnelle, V., Leech, R., Kinnunen, K.M., Ham, T.E., Beckmann, C.F., De Boissezon, X., & Sharp, D.J. (2011). Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. The Journal of Neuroscience, 31(38), 13442–13451. doi:10.1523/JNEUROSCI.1163-11.2011 Google Scholar
Buxton, R.B., Wong, E.C., & Frank, L.R. (1998). Dynamics of blood flow and oxygenation changes during brain activation: The balloon model. Magnetic Resonance in Medicine, 39(6), 855–864.Google Scholar
Caplan, R., & Dapretto, M. (2001). Making sense during conversation: An fMRI study. Neuroreport, 12(16), 3625–3632.Google Scholar
Coleman, M.R., Rodd, J.M., Davis, M.H., Johnsrude, I.S., Menon, D.K., Pickard, J.D., & Owen, A.M. (2007). Do vegetative patients retain aspects of language comprehension? Evidence from fMRI. Brain, 130(Pt 10), 2494–2507. doi:10.1093/brain/awm170 CrossRefGoogle ScholarPubMed
Cox, R.W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162–173.Google Scholar
Dehaene-Lambertz, G., Dehaene, S., & Hertz-Pannier, L. (2002). Functional neuroimaging of speech perception in infants. Science, 298(5600), 2013–2015. doi:10.1126/science.1077066 CrossRefGoogle ScholarPubMed
Demertzi, A., Gomez, F., Crone, J.S., Vanhaudenhuyse, A., Tshibanda, L., Noirhomme, Q., & Soddu, A. (2014). Multiple fMRI system-level baseline connectivity is disrupted in patients with consciousness alterations. Cortex, 52, 35–46. doi:10.1016/j.cortex.2013.11.005 Google Scholar
Di, H.B., Yu, S.M., Weng, X.C., Laureys, S., Yu, D., Li, J.Q., & Chen, Y.Z. (2007). Cerebral response to patient’s own name in the vegetative and minimally conscious states. Neurology, 68(12), 895–899. doi:10.1212/01.wnl.0000258544.79024.d0 Google Scholar
Dronkers, N.F., Wilkins, D.P., Van Valin, R.D. Jr., Redfern, B.B., & Jaeger, J.J. (2004). Lesion analysis of the brain areas involved in language comprehension. Cognition, 92(1-2), 145–177. doi:10.1016/j.cognition.2003.11.002 CrossRefGoogle ScholarPubMed
Fernandez-Espejo, D., Norton, L., & Owen, A.M. (2014). The clinical utility of fMRI for identifying covert awareness in the vegetative state: A comparison of sensitivity between 3T and 1.5T. PLoS One, 9(4), e95082. doi:10.1371/journal.pone.0095082 Google Scholar
Fernandez-Espejo, D., & Owen, A.M. (2013). Detecting awareness after severe brain injury. Nature Reviews Neuroscience, 14(11), 801–809. doi:10.1038/nrn3608 Google Scholar
Giacino, J.T., Ashwal, S., Childs, N., Cranford, R., Jennett, B., Katz, D.I., & Zasler, N.D. (2002). The minimally conscious state definition and diagnostic criteria. Neurology, 58(3), 349–353. doi:10.1212/WNL.58.3.349 CrossRefGoogle ScholarPubMed
Giacino, J.T., Fins, J.J., Laureys, S., & Schiff, N.D. (2014). Disorders of consciousness after acquired brain injury: The state of the science. Nature Reviews Neurology, 10(2), 99–114. doi:10.1038/nrneurol.2013.279 Google Scholar
Giacino, J.T., & Smart, C.M. (2007). Recent advances in behavioral assessment of individuals with disorders of consciousness. Current Opinion in Neurology, 20(6), 614–619. doi:10.1097/WCO.0b013e3282f189ef Google Scholar
Gusnard, D.A., & Raichle, M.E. (2001). Searching for a baseline: Functional imaging and the resting human brain. Nature Reviews Neuroscience, 2(10), 685–694. doi:10.1038/35094500 Google Scholar
Hannawi, Y., Lindquist, M.A., Caffo, B.S., Sair, H.I., & Stevens, R.D. (2015). Resting brain activity in disorders of consciousness: A systematic review and meta-analysis. Neurology, 84(12), 1272–1280. doi:10.1212/WNL.0000000000001404 Google Scholar
Jenkinson, M., Beckmann, C.F., Behrens, T.E., Woolrich, M.W., & Smith, S.M. (2012). Fsl. Neuroimage, 62(2), 782–790. doi:10.1016/j.neuroimage.2011.09.015 Google Scholar
Kalmar, K., & Giacino, J.T. (2005). The JFK Coma Recovery Scale--Revised. Neuropsychological Rehabilitation, 15(3-4), 454–460. doi:10.1080/09602010443000425 Google Scholar
Laureys, S., Lemaire, C., Maquet, P., Phillips, C., & Franck, G. (1999). Cerebral metabolism during vegetative state and after recovery to consciousness. Journal of Neurology, Neurosurgery, and Psychiatry, 67(1), 121.CrossRefGoogle ScholarPubMed
Laureys, S., Owen, A.M., & Schiff, N.D. (2004). Brain function in coma, vegetative state, and related disorders. Lancet Neurology, 3(9), 537–546. doi:10.1016/S1474-4422(04)00852-X Google Scholar
Lutkenhoff, E.S., Rosenberg, M., Chiang, J., Zhang, K., Pickard, J.D., Owen, A.M., & Monti, M.M. (2014). Optimized brain extraction for pathological brains (optiBET). PLoS One, 9(12), e115551. doi:10.1371/journal.pone.0115551 Google Scholar
McKiernan, K.A., Kaufman, J.N., Kucera-Thompson, J., & Binder, J.R. (2003). A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. Journal of Cognitive Neuroscience, 15(3), 394–408. doi:10.1162/089892903321593117 Google Scholar
Monti, M.M., Pickard, J.D., & Owen, A.M. (2013). Visual cognition in disorders of consciousness: From V1 to top-down attention. Human Brain Mapping, 34(6), 1245–1253. doi:10.1002/hbm.21507 Google Scholar
Monti, M.M., Vanhaudenhuyse, A., Coleman, M.R., Boly, M., Pickard, J.D., Tshibanda, L., & Laureys, S. (2010). Willful modulation of brain activity in disorders of consciousness. New England Journal of Medicine, 362(7), 579–589. doi:10.1056/NEJMoa0905370 Google Scholar
Multi-Society Task Force on PVS. (1994). Medical Aspects of the Persistent Vegetative State. New England Journal of Medicine, 330(21), 1499–1508. doi:10.1056/NEJM199405263302107 Google Scholar
Naci, L., & Owen, A.M. (2013). Making every word count for nonresponsive patients. JAMA Neurology, 70(10), 1235–1241. doi:10.1001/jamaneurol.2013.3686 Google Scholar
Owen, A.M., Coleman, M.R., Boly, M., Davis, M.H., Laureys, S., & Pickard, J.D. (2006). Detecting awareness in the vegetative state. Science, 313(5792), 1402. doi:10.1126/science.1130197 Google Scholar
Perani, D., Dehaene, S., Grassi, F., Cohen, L., Cappa, S.F., Dupoux, E., & Mehler, J. (1996). Brain processing of native and foreign languages. Neuroreport, 7(15-17), 2439–2444.Google Scholar
Poldrack, R.A., Mumford, J.A., Schonberg, T., Kalar, D., Barman, B., & Yarkoni, T. (2012). Discovering relations between mind, brain, and mental disorders using topic mapping. PLoS Computational Biology, 8(10), e1002707. doi:10.1371/journal.pcbi.1002707 Google Scholar
Pulvermuller, F., Shtyrov, Y., & Ilmoniemi, R. (2003). Spatiotemporal dynamics of neural language processing: An MEG study using minimum-norm current estimates. Neuroimage, 20(2), 1020–1025. doi:10.1016/S1053-8119(03)00356-2 Google Scholar
Schiff, N.D., Rodriguez-Moreno, D., Kamal, A., Kim, K.H., Giacino, J.T., Plum, F., & Hirsch, J. (2005). fMRI reveals large-scale network activation in minimally conscious patients. Neurology, 64(3), 514–523. doi:10.1212/01.WNL.0000150883.10285.44 CrossRefGoogle ScholarPubMed
Schnakers, C., Vanhaudenhuyse, A., Giacino, J., Ventura, M., Boly, M., Majerus, S., & Laureys, S. (2009). Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment. BMC Neurology, 9, 35. doi:10.1186/1471-2377-9-35 Google Scholar
Stender, J., Gosseries, O., Bruno, M.A., Charland-Verville, V., Vanhaudenhuyse, A., Demertzi, A., & Laureys, S. (2014). Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: A clinical validation study. Lancet, 384(9942), 514–522. doi:10.1016/S0140-6736(14)60042-8 Google Scholar
Teasdale, G., & Jennett, B. (1974). Assessment of coma and impaired consciousness. A practical scale. Lancet, 2(7872), 81–84.Google Scholar
Vanhaudenhuyse, A., Noirhomme, Q., Tshibanda, L.J., Bruno, M.A., Boveroux, P., Schnakers, C., & Boly, M. (2010). Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. Brain, 133(Pt 1), 161–171. doi:10.1093/brain/awp313 CrossRefGoogle ScholarPubMed
Wilson, S.M., Saygin, A.P., Sereno, M.I., & Iacoboni, M. (2004). Listening to speech activates motor areas involved in speech production. Nature Neuroscience, 7(7), 701–702. doi:10.1038/nn1263 Google Scholar
Yarkoni, T., Poldrack, R.A., Nichols, T.E., Van Essen, D.C., & Wager, T.D. (2011). Large-scale automated synthesis of human functional neuroimaging data. Nature Methods, 8(8), 665–670. doi:10.1038/nmeth.1635 Google Scholar