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Functional Neuroimaging of Disorders of Consciousness

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Functional Neuroimaging of Disorders of Consciousness Functional Neuroimaging of Disorders of Consciousness Martin R. Coleman, PhD* Adrian M. Owen, PhD*w Wolfson Brain Imaging Centre, Addenbrookes Hospital MRC Cognition and Brain Sciences Unit An accurate and reliable evaluation of the level and content of cognitive processing is of paramount importance for the appropriate management of severely brain-damaged patients with disorders of consciousness.1 Objective behavioral assessment of residual cognitive function can be extremely challenging in these patients, as motor responses may be minimal, inconsistent, and difficult to document, or may be undetectable because no cognitive output is possible. This difficulty leads to much confusion and a high-level of misdiagnoses in the vegetative state (VS), minimally conscious state, and locked-in syndrome.2,3 Recent advances in functional neuroimaging suggest a novel solution to this problem; so-called ‘‘activation’’ studies can be used to assess cognitive functions in altered states of consciousness without the need for any overt response on the part of the patient. In several recent studies, this approach has been used to detect residual cognitive function and even conscious awareness in patients who behaviorally meet the criteria defining the VS.4–6 Similarly, these techniques have been used in other studies to guide therapeutic interventions and track recovery processes.7,8 Such studies suggest that the future integration of emerging functional neuroimaging techniques with existing clinical and behavioral methods of assessment will be essential in reducing the current rate of misdiagnosis. Moreover, such FROM THE *CAMBRIDGE IMPAIRED CONSCIOUSNESS RESEARCH GROUP,WOLFSON BRAIN IMAGING CENTRE, ADDENBROOKES HOSPITAL AND THE wMRC COGNITION AND BRAIN SCIENCES UNIT REPRINTS:MARTIN R. COLEMAN,PHD, CAMBRIDGE IMPAIRED CONSCIOUSNESS RESEARCH GROUP,WOLFSON BRAIN IMAGING CENTRE,BOX 65, ADDENBROOKES HOSPITAL,CAMBRIDGE CB2 0QQ, UK, E-MAIL:[email protected] INTERNATIONAL ANESTHESIOLOGY CLINICS Volume 46, Number 3, 147–157 r 2008, Lippincott Williams & Wilkins 147 148 ’ Coleman and Owen efforts may provide important new prognostic indicators, helping to disentangle differences in outcome on the basis of a greater under- standing of the underlying mechanisms responsible and better guiding therapeutic choices in these challenging populations.9,10 ’ Positron Emission Tomography Until recently, the majority of neuroimaging studies in patients with disorders of consciousness used either flurodeoxyglucose positron emission tomography (PET) or single photon emission computed tomography to measure resting cerebral blood flow and glucose metabolism.11–15 Typically, widespread reductions in metabolic activity of up to 50% were reported, although, in some studies, normal cerebral metabolism or blood flow in patients in a VS has also been reported.16,17 In some cases, isolated ‘‘islands’’ of metabolism were identified in circumscribed regions of cortex, suggesting residual cognitive proces- sing in a subset of patients.16 In 1 recent and remarkable case of late recovery from minimally conscious state, longitudinal PET examinations revealed increases in resting metabolism coincident with marked clinical improvements in motor function.8 Although metabolic studies are useful in this regard, they can only identify functionality at the most general level; that is, mapping cortical and subcortical regions that are potentially recruitable, rather than relating neural activity within such regions to specific cognitive processes. On the other hand, methods such 15 as H2 O PET and functional magnetic resonance imaging (fMRI) can be used to link distinct and specific physiologic responses (changes in regional cerebral blood flow or changes in regional cerebral hemody- namics) to specific cognitive processes in the absence of any overt response (eg, a motor action or a verbal response) on the part of the patient.18 Early activation studies in patients with disorders of consciousness 15 used H2 O PET, in part because the technique was more widely available and in part because the multiple logistic difficulties of scanning critically ill patients in the strong magnetic field that is integral to fMRI studies 15 had yet to be resolved. In the first of such studies, H2 O PET was used to measure regional cerebral blood flow in a posttraumatic vegetative patient during an auditorily presented story told by his mother.19 Compared with nonword sounds, activation was observed in the anterior cingulate and temporal cortices, possibly reflecting emotional processing of the contents, or tone, of the mother’s speech. In another patient diagnosed as vegetative, Menon et al20 used PET to study covert visual processing in response to familiar faces. When the patient was presented with pictures of the faces of family and close friends, robust activity was observed in the right fusiform gyrus, the so-called human Functional Neuroimaging of Disorders of Consciousness ’ 149 ‘‘face area.’’ Importantly, both of these studies involved single, well- documented cases; in cohort PET studies of patients unequivocally meeting the clinical diagnosis of the VS, normal brain activity in response to external stimulation has generally been the exception rather than the rule. For example, in 1 study of 15 VS patients, high- intensity noxious electrical stimulation activated midbrain, contralateral thalamus, and primary somatosensory cortex in every patient.21 However, unlike control subjects, the patients did not activate secondary somatosensory, insular, posterior parietal, or anterior cingulate cortices. 15 H2 O PET studies are limited by issues of radiation burden that may preclude essential longitudinal or follow-up studies in many patients or even a comprehensive examination of multiple cognitive processes within any one session. The power of PET studies to detect statistically significant responses is also low and group studies are often needed to satisfy standard statistical criteria.18 Given the heterogeneous nature of disorders of consciousness and the clinical need to define each individual in terms of their diagnosis, residual functions, and potential for recovery, such limitations are of paramount importance in the evaluation of these patients. A significant development in this rapidly evolving field has been 15 the relative shift of emphasis from PET ‘‘activation studies’’ using H2 O methodology to fMRI. Not only is magnetic resonance imaging more widely available than PET, it offers increased statistical power, improved spatial and temporal resolution, and has no associated radiation burden. ’ fMRI Event-related fMRI has so far been used to reveal various degrees of retained speech comprehension in patients with disorders of conscious- ness.4,22–24 However, fMRI is not without its complexities and challenges when applied to this patient group. Although it is possible to present visual, tactile, and noxious stimuli in the magnetic resonance imaging environment, to date only auditory stimuli have been used in this context. Work in a strong magnetic field has well-known safety and logistical constraints, but the behavioral portfolio of patients with disorders of consciousness also creates challenges. For example, many vegetative patients only have transient periods of eye opening precluding the use of visual paradigms. Similarly, scanning a patient who is unable to communicate presents numerous ethical dilemmas, particularly when they are unable to tell you if they are in pain. Where these difficulties are overcome, however, the design of fMRI paradigms and their interpretation must also be carefully planned to ensure that a specific cognitive process is targeted and where neural activation is observed this is known to be anatomically and 150 ’ Coleman and Owen physiologically appropriate in healthy volunteers. Unfortunately, many neuroimaging paradigms are let down by the use of a reverse inference approach, whereby a given cognitive process is inferred solely on the basis of an observed activation in a particular brain region. For instance, a patient is presented with his/her name spoken by the voice of his/her mother in 1 condition and the sound of scanner noise in another condition. Using a simple subtraction analysis, the experimenters observe greater cortical activation in the primary auditory cortex when the patient hears his mother’s voice versus the scanner noise. One conclusion could be that the patient recognized his/her name, but the activation observed could equally reflect a low-level orienting response to speech in general or an emotional response to the mother’s voice. Consequently, such a paradigm lacks cognitive specificity and, therefore, provides limited information about the retained cognitive function of a patient with impaired consciousness. fMRI paradigms, therefore, require careful planning to ensure that they are appropriately counter- balanced and can be directly attributed to a specific cognitive process under study. Using mother’s voice as an example, a study by Staffen et al23 compared the response of a patient to hearing their own name versus another name. In this case, because identical speech stimuli were used that differed only with respect to the name itself, activations can be confidently attributed to cognitive processing that is specifically related to the patient’s own name. Staffen and colleagues found activation in the medial prefrontal cortex in response to the patient’s own, but not in response to other names. This pattern of activation was similar to that observed in 3 healthy
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