Disentangling Disorders of Consciousness: Insights from Diffusion Tensor Imaging and Machine Learning

Overview

Journal Hum Brain Mapp

Publisher Wiley

Specialty Neurology

Date 2016 Sep 14

PMID 27622575

Citations 42

Authors

Zhong S Zheng

Nicco Reggente

Evan Lutkenhoff

Adrian M Owen

Martin M Monti

Affiliations

Soon will be listed here.

Abstract

Previous studies have suggested that disorders of consciousness (DOC) after severe brain injury may result from disconnections of the thalamo-cortical system. However, thalamo-cortical connectivity differences between vegetative state (VS), minimally conscious state minus (MCS-, i.e., low-level behavior such as visual pursuit), and minimally conscious state plus (MCS+, i.e., high-level behavior such as language processing) remain unclear. Probabilistic tractography in a sample of 25 DOC patients was employed to assess whether structural connectivity in various thalamo-cortical circuits could differentiate between VS, MCS-, and MCS+ patients. First, the thalamus was individually segmented into seven clusters based on patterns of cortical connectivity and tested for univariate differences across groups. Second, reconstructed whole-brain thalamic tracks were used as features in a multivariate searchlight analysis to identify regions along the tracks that were most informative in distinguishing among groups. At the univariate level, it was found that VS patients displayed reduced connectivity in most thalamo-cortical circuits of interest, including frontal, temporal, and sensorimotor connections, as compared with MCS+, but showed more pulvinar-occipital connections when compared with MCS-. Moreover, MCS- exhibited significantly less thalamo-premotor and thalamo-temporal connectivity than MCS+. At the multivariate level, it was found that thalamic tracks reaching frontal, parietal, and sensorimotor regions, could discriminate, up to 100% accuracy, across each pairwise group comparison. Together, these findings highlight the role of thalamo-cortical connections in patients' behavioral profile and level of consciousness. Diffusion tensor imaging combined with machine learning algorithms could thus potentially facilitate diagnostic distinctions in DOC and shed light on the neural correlates of consciousness. Hum Brain Mapp 38:431-443, 2017. © 2016 Wiley Periodicals, Inc.

Citing Articles

A light in the darkness: Early phases of development and the emergence of cognition.

Cainelli E, Stramucci G, Bisiacchi P Dev Cogn Neurosci. 2025; 72:101527.

PMID: 39933251 PMC: 11869870. DOI: 10.1016/j.dcn.2025.101527.

Relationship between δ-catenin expression and whole-brain small-world network in breast cancer patients before chemotherapy.

Xue M, Du W, Cao J, Jiang Y, Song D, Yu D Sci Rep. 2024; 14(1):31119.

PMID: 39730828 PMC: 11681013. DOI: 10.1038/s41598-024-82391-x.

Revolutionizing treatment for disorders of consciousness: a multidisciplinary review of advancements in deep brain stimulation.

Yang Y, Cao T, He S, Wang L, He Q, Fan L Mil Med Res. 2024; 11(1):81.

PMID: 39690407 PMC: 11654023. DOI: 10.1186/s40779-024-00585-w.

Explaining recovery from coma with multimodal neuroimaging.

Pozeg P, Johr J, Prior J, Diserens K, Dunet V J Neurol. 2024; 271(9):6274-6288.

PMID: 39090230 PMC: 11377522. DOI: 10.1007/s00415-024-12591-y.

Re-awakening the brain: Forcing transitions in disorders of consciousness by external in silico perturbation.

Dagnino P, Escrichs A, Lopez-Gonzalez A, Gosseries O, Annen J, Sanz Perl Y PLoS Comput Biol. 2024; 20(5):e1011350.

PMID: 38701063 PMC: 11068192. DOI: 10.1371/journal.pcbi.1011350.

References

Monti M, Laureys S, Owen A . The vegetative state. BMJ. 2010; 341:c3765. DOI: 10.1136/bmj.c3765. View

Smith S . Fast robust automated brain extraction. Hum Brain Mapp. 2002; 17(3):143-55. PMC: 6871816. DOI: 10.1002/hbm.10062. View

Fernandez-Espejo D, Bekinschtein T, Monti M, Pickard J, Junque C, Coleman M . Diffusion weighted imaging distinguishes the vegetative state from the minimally conscious state. Neuroimage. 2010; 54(1):103-12. DOI: 10.1016/j.neuroimage.2010.08.035. View

Bruno M, Vanhaudenhuyse A, Thibaut A, Moonen G, Laureys S . From unresponsive wakefulness to minimally conscious PLUS and functional locked-in syndromes: recent advances in our understanding of disorders of consciousness. J Neurol. 2011; 258(7):1373-84. DOI: 10.1007/s00415-011-6114-x. View

Pereira F, Mitchell T, Botvinick M . Machine learning classifiers and fMRI: a tutorial overview. Neuroimage. 2008; 45(1 Suppl):S199-209. PMC: 2892746. DOI: 10.1016/j.neuroimage.2008.11.007. View

Schiff N, Giacino J, Kalmar K, Victor J, Baker K, Gerber M . Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature. 2007; 448(7153):600-3. DOI: 10.1038/nature06041. View

Laureys S, Faymonville M, Luxen A, Lamy M, FRANCK G, Maquet P . Restoration of thalamocortical connectivity after recovery from persistent vegetative state. Lancet. 2000; 355(9217):1790-1. DOI: 10.1016/s0140-6736(00)02271-6. View

Jennett B, Adams J, Murray L, Graham D . Neuropathology in vegetative and severely disabled patients after head injury. Neurology. 2001; 56(4):486-90. DOI: 10.1212/wnl.56.4.486. View

Laureys S . The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn Sci. 2005; 9(12):556-9. DOI: 10.1016/j.tics.2005.10.010. View

10.

Yamamoto T, Katayama Y . Deep brain stimulation therapy for the vegetative state. Neuropsychol Rehabil. 2005; 15(3-4):406-13. DOI: 10.1080/09602010443000353. View

11.

Smith S, Nichols T . Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2008; 44(1):83-98. DOI: 10.1016/j.neuroimage.2008.03.061. View

12.

Childs N, Mercer W . Misdiagnosing the persistent vegetative state. Misdiagnosis certainly occurs. BMJ. 1996; 313(7062):944. PMC: 2352258. DOI: 10.1136/bmj.313.7062.944. View

13.

Dehaene S, Changeux J . Experimental and theoretical approaches to conscious processing. Neuron. 2011; 70(2):200-27. DOI: 10.1016/j.neuron.2011.03.018. View

14.

Monti M, Rosenberg M, Finoia P, Kamau E, Pickard J, Owen A . Thalamo-frontal connectivity mediates top-down cognitive functions in disorders of consciousness. Neurology. 2014; 84(2):167-73. PMC: 4336082. DOI: 10.1212/WNL.0000000000001123. View

15.

Tsubokawa T, Yamamoto T, Katayama Y, Hirayama T, Maejima S, Moriya T . Deep-brain stimulation in a persistent vegetative state: follow-up results and criteria for selection of candidates. Brain Inj. 1990; 4(4):315-27. DOI: 10.3109/02699059009026185. View

16.

Kanno T, Kamei Y, Yokoyama T, Jain V . Neurostimulation for patients in vegetative status. Pacing Clin Electrophysiol. 1987; 10(1 Pt 2):207-8. DOI: 10.1111/j.1540-8159.1987.tb05949.x. View

17.

Laureys S, Goldman S, Phillips C, Van Bogaert P, Aerts J, Luxen A . Impaired effective cortical connectivity in vegetative state: preliminary investigation using PET. Neuroimage. 1999; 9(4):377-82. DOI: 10.1006/nimg.1998.0414. View

18.

Behrens T, Johansen-Berg H, Woolrich M, Smith S, Wheeler-Kingshott C, Boulby P . Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 2003; 6(7):750-7. DOI: 10.1038/nn1075. View

19.

Kriegeskorte N, Goebel R, Bandettini P . Information-based functional brain mapping. Proc Natl Acad Sci U S A. 2006; 103(10):3863-8. PMC: 1383651. DOI: 10.1073/pnas.0600244103. View

20.

Bruno M, Majerus S, Boly M, Vanhaudenhuyse A, Schnakers C, Gosseries O . Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients. J Neurol. 2011; 259(6):1087-98. DOI: 10.1007/s00415-011-6303-7. View