Detecting Awareness in the Vegetative State BREVIA
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BREVIA imagine playing tennis, significant activity was observed in the supplementary motor area (Fig. 1). In contrast, when she was asked to im- Detecting Awareness in the agine walking through her home, significant activity was observed in the parahippocampal gyrus, the posterior parietal cortex, and the lateral Vegetative State premotor cortex (Fig. 1). Her neural responses were indistinguishable from those observed in Adrian M. Owen,1* Martin R. Coleman,2 Melanie Boly,3 Matthew H. Davis,1 healthy volunteers (fig. S2) performing the same Steven Laureys,3 John D. Pickard2 imagery tasks in the scanner (SOM text). These results confirm that, despite fulfilling he vegetative state is one of the least un- from a beam in the ceiling[) produced an ad- the clinical criteria for a diagnosis of vegetative derstood and most ethically troublesome ditional significant response in a left inferior state, this patient retained the ability to under- Tconditions in modern medicine. The term frontal region, similar to that observed for normal stand spoken commands and to respond to them describes a unique disorder in which patients volunteers. This increased activity for ambiguous through her brain activity, rather than through who emerge from coma appear to be awake but sentences reflects the operation of semantic pro- speech or movement. Moreover, her decision to show no signs of awareness. Although the cesses that are critical for speech comprehension. cooperate with the authors by imagining partic- diagnosis depends crucially on there being no An appropriate neural response to the mean- ular tasks when asked to do so represents a clear reproducible evidence of purposeful behavior in ing of spoken sentences, although suggestive, is act of intention, which confirmed beyond any response to external stimulation (1), recent func- not unequivocal evidence that a person is con- doubt that she was consciously aware of herself tional neuroimaging studies have suggested that sciously aware. For example, many studies of and her surroundings. Of course, negative find- Bislands[ of preserved brain function may exist implicit learning and priming, as well as studies ings in such patients cannot be used as evidence in a small percentage of patients who have been of learning during anesthesia and sleep, have for lack of awareness, because false negative diagnosed as vegetative (2). On this basis, we demonstrated that aspects of human cognition, findings in functional neuroimaging studies are hypothesized that this technique also may pro- including speech perception and semantic pro- common, even in healthy volunteers. However, vide a means for detecting conscious awareness cessing, can go on in the absence of conscious in the case described here, the presence of re- on August 29, 2010 in patients who are assumed to be vegetative awareness. producible and robust task-dependent responses yet retain cognitive abilities that have evaded To address this question of conscious aware- to command without the need for any practice or detection using standard clinical methods. ness, we conducted a second fMRI study during training suggests a method by which some non- In July 2005, a 23-year-old woman sustained a which the patient was given spoken instructions communicative patients, including those diag- severe traumatic brain injury as a result of a road to perform two mental imagery tasks at specific nosed as vegetative, minimally conscious, or traffic accident. Five months later, she remained points during the scan (3). One task involved locked in, may be able to use their residual cog- unresponsive with preserved sleep-wake cycles. imagining playing a game of tennis and the nitive capabilities to communicate their thoughts Clinical assessment by a multidisciplinary team other involved imagining visiting all of the to those around them by modulating their own concluded that she fulfilled all of the criteria for a rooms of her house, starting from the front neural activity. www.sciencemag.org diagnosis of vegetative state according to inter- door. During the periods that she was asked to national guidelines (1) References and Notes ESupporting Online Ma- 1. Royal College of Physicians, The Vegetative State: Guidance ^ on Diagnosis and Management (Report of a Working Party, terial (SOM) text . Royal College of Physicians, London, 2003). We used function- 2. N. D. Schiff et al., Brain 125, 1210 (2002). al magnetic resonance 3. Materials and methods are available as supporting imaging (fMRI) to mea- material on Science Online. 4. We thank D. Badwan, T. Bekinschtein, J. Rodd, J. Outtrim, Downloaded from sure her neural responses D. Chatfield, D. Menon, I. Johnsrude, V. Lupson, R. Barker, during the presentation J. Grahn, C. Frith, P. Maquet, the Cambridge Impaired of spoken sentences Consciousness Research Group, and the staff of the (e.g., BThere was milk Wellcome Trust Research Facility for their contributions. and sugar in his cof- Funded by MRC program grant G9439390 ID 56833, the [ Smiths Charity, the Belgian Fonds National de la fee ), which were com- Recherche Scientifique, and the Mind Science Foundation. pared with responses Supporting Online Material to acoustically matched www.sciencemag.org/cgi/content/full/313/5792/1402/DC1 noise sequences (3). Materials and Methods Speech-specific activi- SOM Text ty was observed bilat- Figs. S1 and S2 References erally in the middle and superior temporal gyri, 19 May 2006; accepted 17 July 2006 10.1126/science.1130197 equivalent to that ob- served in healthy vol- 1Medical Research Council Cognition and Brain Sciences Fig. 1. We observed supplementary motor area (SMA) activity during tennis 2 unteers listening to the imagery in the patient and a group of 12 healthy volunteers (controls). We Unit, Cambridge CB2 2EF, UK. Division of Academic same stimuli (fig. S1). Neurosurgery, Addenbrooke’s Hospital and Wolfson Brain detected parahippocampal gyrus (PPA), posterior parietal-lobe (PPC), and Imaging Centre, University of Cambridge, Cambridge CB2 Furthermore, sentences lateral premotor cortex (PMC) activity while the patient and the same group of 2QQ, UK. 3Cyclotron Research Centre and Neurology that contained ambigu- volunteers imagined moving around a house. All results are thesholded at P G Department, University of Lie`ge, 4000 Lie`ge, Belgium. ous words (italicized) 0.05 corrected for multiple comparisons. X values refer to distance in mm *To whom correspondence should be addressed. E-mail: (e.g., BThe creak came from the midline in stereotaxic space (SOM text). [email protected] 1402 8 SEPTEMBER 2006 VOL 313 SCIENCE www.sciencemag.org.