Executive functions in the absence of behavior: functional imaging of the minimally conscious state

doi:10.1016/S0079-6123(09)17717-8

Progress in Brain Research

Volume 177, 2009, Pages 249-260

https://doi.org/10.1016/S0079-6123(09)17717-8 Get rights and content

Abstract

One of the major challenges in the clinical evaluation of brain injury survivors is to comprehensively assess the level of preserved cognitive function in order to inform diagnostic decisions and suggest appropriate rehabilitation strategies. However, the limited (if any) capacity for producing behavior in some of these patients often limits the extent to which cognitive functions can be explored via standard bedside methods. We present a novel neuroimaging paradigm that allows the assessment of residual executive functions without requiring the patient to produce any behavioral output. In particular, we target processes such as active maintenance of information through time and willful adoption of “mind-sets” that have been proposed to require conscious awareness. Employing an fMRI block design paradigm, healthy volunteers were presented with a series of neutral (i.e., not emotionally salient) words, and alternatively instructed to listen to all the words, or to count the number of times a given target is repeated. Importantly, the perceptual stimulation in the passive listening and the counting tasks was carefully matched. Contrasted with passive listening, the counting task revealed a fronto-parietal network previously associated with target detection and working memory. Remarkably, when tested on this same procedure, a minimally conscious patient presented a highly similar pattern of activation. Furthermore, the activity in these regions appeared highly synchronous to the onset and offset of the counting blocks. Considering the close matching of sensory stimulation across the two tasks, these findings strongly suggest that the patient could willfully adopt differential “mind-sets” as a function of condition, and could actively maintain information across time. Neither cognitive function was apparent when the patient was (behaviorally) tested at the bedside. This paradigm thus exemplifies the potential for fMRI to explore high-level cognitive functions, and awareness, in the absence of any behavioral response.

Section snippets

Participants

Twenty healthy volunteers (12 female) with no history of neurological disorder and one MCS patient participated in the experiment. Healthy volunteers signed informed consent prior to the experimental session. For the patient, assent was obtained from the next of kin. This study was approved by the Cambridge Local Research Ethics Committee.

Patient history

The patient was first hospitalized on October 28, 2007 after suffering a cardio-respiratory arrest, and was resuscitated in ITU (defibrillated/intubated and

Healthy volunteers

Averaging across all healthy volunteers, the target detection versus passive listening contrast revealed activations spanning frontal, temporal, and parietal cortex, along with regions of the cerebellum (see Table 1 and Fig. 2). Frontal cortex was activated bilaterally in the sub-lobar sections of the inferior frontal gyrus (BA 47), and in the middle frontal gyrus (BA 10). Activation was also observed in the right superior frontal (BA 10) and cingulate gyri (BA 32), left precentral gyrus (BA

Discussion

Compared to simple listening, the counting task elicited, in all healthy volunteers, a pattern of activation similar to that reported in previous studies of executive function, including target detection and working memory (see Naghavi and Nyberg, 2005). The very fact that the two (perceptually identical) tasks elicited different patterns of activation confirms that our paradigm does elicit the expected cognitive processes including maintenance of information through time and willful adoption

Conclusions

Detecting consciousness in brain injury survivors is critical for appropriate diagnosis and patient management (Bernat, 2006). Objective assessment on the basis of observed and elicited behavior, however, can be extremely challenging in patients with little ability for behavioral output. Use of noninvasive neuroimaging techniques to detect residual cognitive abilities and awareness may thus be crucial to reducing diagnostic error (Owen and Coleman, 2008). While there is at present limited

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DOC are commonly assessed in the clinical practice using such tools as the Coma Recovery Scale–Revised (CRS-R; Giacino et al., 2004), which is primarily based on the patients’ behavioural responsiveness to stimuli. However, several aspects of awareness could be preserved in chronic DOC patients in the absence of an explicit behavioural interaction with the environment (Andrews et al., 1996; Childs et al., 1993; Demertzi et al., 2008; Eickhoff et al., 2008; Fernandez-Espejo et al., 2008; Giacino et al., 2009; Majerus et al., 2005; Monti et al., 2009; Owen et al., 2002, 2006, 2005; Rosanova et al., 2012; Schnakers et al., 2009). For instance, in a seminal study, Owen and colleagues (2006) used a motor imagery paradigm during fMRI to detect the neural correlates of command-following in one patient diagnosed as behaviourally vegetative.
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Executive functions in the absence of behavior: functional imaging of the minimally conscious state

Abstract

Section snippets

Participants

Patient history

Healthy volunteers

Discussion

Conclusions

Trends in Cognitive Sciences

Trends in Neurosciences

NeuroImage

Lancet

Trends in Cognitive Sciences

Cognition

NeuroImage

Archives of Physical Medicine and Rehabilitation

Journal of Chemical Neuroanatomy

NeuroImage

Medical Image Analysis

Trends in Cognitive Sciences

NeuroImage

Lancet Neurology

Consciousness and Cognition

Progress in Brain Research

Consciousness and Cognition

Neuroscience Letters

Trends in Cognitive Sciences

NeuroImage

Neuropsychologia

NeuroImage

NeuroImage

Misdiagnosis of the vegetative state: Retrospective study in a rehabilitation unit

British Medical Journal