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Original Investigation |

Making Every Word Count for Nonresponsive Patients

Lorina Naci, PhD1; Adrian M. Owen, PhD1
[+] Author Affiliations
1The Brain and Mind Institute, Department of Psychology, Western University, London, Ontario, Canada
JAMA Neurol. 2013;70(10):1235-1241. doi:10.1001/jamaneurol.2013.3686.
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Importance  Despite the apparent absence of external signs of consciousness, a significant small proportion of patients with disorders of consciousness can respond to commands by willfully modulating their brain activity, even respond to yes or no questions, by performing mental imagery tasks. However, little is known about the mental life of such responsive patients, for example, with regard to whether they can have coherent thoughts or selectively maintain attention to specific events in their environment. The ability to selectively pay attention would provide evidence of a patient’s preserved cognition and a method for brain-based communication, thus far untested with functional magnetic resonance imaging in this patient group.

Objective  To test whether selective auditory attention can be used to detect conscious awareness and communicate with behaviorally nonresponsive patients.

Design, Setting, and Participants  Case study performed in 3 patients with severe brain injury, 2 diagnosed as being in a minimally conscious state and 1 as being in a vegetative state. The patients constituted a convenience sample.

Main Outcomes and Measures  Functional magnetic resonance imaging data were acquired as the patients were asked to selectively attend to auditory stimuli, thereby conveying their ability to follow commands and communicate.

Results  All patients demonstrated command following according to instructions. Two patients (1 in a minimally conscious state and 1 in a vegetative state) were also able to guide their attention to repeatedly communicate correct answers to binary (yes or no) questions.

Conclusions and Relevance  To our knowledge, we show for the first time with functional magnetic resonance imaging that behaviorally nonresponsive patients can use selective auditory attention to convey their ability to follow commands and communicate. One patient in a minimally conscious state was able to use attention to establish functional communication in the scanner, despite his inability to produce any communication responses in repeated bedside examinations. More important, 1 patient, who had been in a vegetative state for 12 years before the scanning and subsequent to it, was able to use attention to correctly communicate answers to several binary questions. The technique may be useful in establishing basic communication with patients who appear unresponsive to bedside examinations and cannot respond with existing neuroimaging methods.

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Figure 1.
Region-of-Interest Data for 1 Patient in a Minimally Conscious State

The parietal and prefrontal regions of interest are displayed on the patient’s native anatomic volume. From left to right, in purple or light purple are the T-score values for the brain activity in the 2 regions of interest during the command-following and localizer scan. By default, these were significant. In black and gray are the T-score values for question 1 and question 2 (contrast yes-no). Positive values represent higher brain activity for yes than for no word sequences and vice versa. Significant T-score values are indicated by a red asterisk. The direction of significant functional activation (ie, yes > no or no > yes) indicated an answer of yes or no. These are displayed at the bottom of the graph. Green indicates a correct match to the factual answers.

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Figure 2.
Command Following and Communication for 1 Patient in a Minimally Conscious State

Command-following (A) and communication (B and C) scans in patient 2, who was clinically diagnosed as being in a minimally conscious state. The brain activity is overlaid on the patient’s native anatomic volume. The opposite directions of each contrast (ie, a > b or b > a) are shown on the left and right sides of each panel. A, The command-following scan also served to localize the brain foci of attention, unique to the patient. B and C, Selective attention to one of the answer words (either yes or no) during each communication scan was investigated within these regions. Attention to answering questions B (yes) and C (no) significantly activated the frontotemporal and parietal regions, respectively.

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Figure 3.
Region-of-Interest Data for the Patient in a Vegetative State

The precentral and temporal regions of interest are displayed on the patient’s structural scan in the upper left of the figure. From left to right, in blue and light blue are the T-score values for the brain activity in the 2 regions of interest during the command-following and localizer scan. By default, these were significant. In black and gray are the T-score values for question 1 and question 2, for visits 1 and 2 (contrast: yes-no). The same regions of interest were used to decode the answers to the questions in the 2 visits. Positive values represent higher activity (T-score values) for yes than no and vice versa. Significant T-score values are indicated by a red asterisk. The direction of significant functional activation indicated an answer of yes or no. These are displayed at the bottom of the graph. Green indicates a correct match to the factual answers.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 4.
Command-Following and Communication Scans for the Patient in a Vegetative State

Command-following (A) and communication (B and C) scans in patient 3, clinically diagnosed as being in a vegetative state. Brain activity is overlaid on the patient’s native anatomic volume. The opposite directions of each contrast (ie, a > b or b > a) are shown on the left and right sides of each panel. A, The command-following scan also served to localize the brain foci of attention unique to the patient. B and C, Selective attention to the answer word (either yes or no) during each communication scan was investigated within these regions. Attention to the answer in each question (B, no; C, yes) significantly activated the precentral or motor region.

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