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Massimini PBR Coma Science 2009

Massimini PBR Coma Science 2009

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S. Laureys et al. (Eds.)Progress in Brain Research
, Vol. 177ISSN 0079-6123Copyright
2009 Elsevier B.V. All rights reserved
A perturbational approach for evaluating the brain’scapacity for consciousness
Marcello Massimini
, Melanie Boly
, Adenauer Casali
, Mario Rosanova
andGiulio Tononi
Department of Clinical Sciences, University of Milan, Milan, Italy
Coma Science Group, Cyclotron Research Center and Neurology Department, University of Liege andCHU Hospital, Belgium
Department of Psychiatry, University of Wisconsin, WI, USA
How do we evaluate a brain’s capacity to sustain conscious experience if the subject does notmanifest purposeful behaviour and does not respond to questions and commands? What should wemeasure in this case? An emerging idea in theoretical neuroscience is that what really matters forconsciousness in the brain is not activity levels, access to sensory inputs or neural synchronization per se,but rather the ability of different areas of the thalamocortical system to interact causally with each otherto form an integrated whole. In particular, the information integration theory of consciousness (IITC)argues that consciousness is integrated information and that the brain should be able to generateconsciousness to the extent that it has a large repertoire of available states (
), yet it cannot bedecomposed into a collection of causally independent subsystems (
). To evaluate the ability tointegrate information among distributed cortical regions, it may not be sufficient to observe the brain inaction. Instead, it is useful to employ a perturbational approach and examine to what extent differentregions of the thalamocortical system can interact causally (
) and produce specific responses(
). Thanks to a recently developed technique, transcranial magnetic stimulation and high-density electroencephalography (TMS/hd-EEG), one can record the immediate reaction of the entirethalamocortical system to controlled perturbations of different cortical areas. In this chapter, using sleepas a model of unconsciousness, we show that TMS/hd-EEG can detect clear-cut changes in the ability of the thalamocortical system to integrate information when the level of consciousness fluctuates across thesleep–wake cycle. Based on these results, we discuss the potential applications of this novel technique toevaluate objectively the brain’s capacity for consciousness at the bedside of brain-injured patients.
coma; consciousness; transcranial magnetic stimulation; electroencephalography; information;integration
Evaluating a subject’s level of consciousness
The bedside evaluation of patients affected by
Corresponding author.
disorders of consciousness (DOC) relies on
Tel.: +39 33 39 92 57 91; Fax: +39 02 48002084;E-mail: marcello.massimini@unimi.it
repeated behavioural observation by trained
personnel. During the examination, spontaneousand elicited behaviour in response to multisensorystimulation is recorded in accordance with specificscales (Giacino et al., 2004;Gill-Thwaites and  Munday, 2004;Kalmar and Giacino, 2005;Shiel  et al., 2000). Regardless of the scale employed,the examiner typically looks for (1) evidence of awareness of the self or of the environment, (2)evidence of sustained, reproducible, purposeful orvoluntary response to tactile, auditory or noxiousstimuli and (3) evidence of language comprehension and expression (Laureys et al., 2004). If noneof these three defining behavioural features canbe detected during careful and repeated evaluations, the subject is considered unconscious(Royal College of Physicians, 1994), whilepatients who show non-reflexive behaviour butare unable to communicate their thoughts andfeelings are ascribed to a recently defined clinicalentity, the minimally conscious state (Giacino et al., 2002). Thus, according to the clinicaldefinition of consciousness, subjects are consciousif they can signal that this is the case. However,since in patients with severe brain injury motorresponsiveness is often impaired, it may alsohappen that a subject is aware but unable tomove or speak (Schnakers et al., 2009). Therefore,while detecting the presence of voluntary behaviour at the bedside is sufficient to infer that asubject is aware, its absence does not necessarilyimply unconsciousness (Boly et al., 2007;Laureys  et al., 2004;Monti et al., 2009). Recently, the development of new neuroimaging protocols has made it possible to probe forsigns of awareness even when subjects arecompletely unable to move (Boly et al., 2007;Owen and Coleman, 2008). For example, in arecent study (Owen and Coleman, 2008), aclinically vegetative, seemingly unresponsivepatient was put in the scanner and asked toimagine playing tennis or navigating through herown apartment. Remarkably, the patient showedfMRI patterns of brain activation that wereconsistent and specific for the requested cognitivetask, just like healthy subjects. This paradigmaticcase demonstrates that the patient’s ability towilfully enter specific neural states upon requestcan be used to detect the presence of awarenesseven when motor outputs are absent. However,there still may be cases, such as in aphasia,akinetic mutism, catatonic depression or diffusedopaminergic lesions, where a patient, althoughaware, may not be able to understand or bewilling to respond (Boly et al., 2007). Moreover,because of frequent movement artefacts andbecause of possible alterations of the normalcoupling of hemodynamics and neuronal firing(Rossini et al., 2004), acquiring and interpretingfMRI data is especially difficult in DOC patients(Giacino et al., 2006). Hence, the absence of volitional brain activity in the scanner, just like theabsence of purposeful movements during aclinical examination, does not necessarily implythe absence of awareness.The behavioural approach and the neuroimaging paradigm represent two different levels atwhich a communication can be established with aDOC patient (Owen et al., 2005). If an overtbehaviour fails to signal consciousness, it is stillpossible to dig deeper by looking for purposefulneural activations. Both methods leave no doubtsin case of a positive result: if the subjects respond,they are actually aware. Instead, a negative resultleaves an open question.
Evaluating a brain’s capacity for consciousness
In this chapter, we propose an additional level atwhich consciousness can be studied even when nocommunication whatsoever (behavioural orneural) can be established with the subject. Thisparadigm does not aim at probing the subject inorder to elicit wilfull behaviours or neural activations; rather, it involves probing directly thesubject’s brain to gauge core properties that aretheoretically relevant for consciousness. Thisoption requires (1) starting from a theory thatsuggests which properties are fundamental for aphysical system to give rise to conscious experience and (2) identifying and implementing apractical measuring method to weigh up theseproperties in a real brain. Here, we start with theinformation integration theory of consciousness (IITC) (Tononi, 2004, 2005, 2008), a theorythat argues that consciousness is integrated
information and that a physical system should beable to generate consciousness to the extent that itcan enter any of a large number of available states(
), yet it cannot be decomposed into acollection of causally independent subsystems(
). Then, we devise a practical methodto gauge the brain’s capacity to integrate information. To do this we employ a combination of transcranial magnetic stimulation and electroencephalography (TMS/hd-EEG), a technique thatallows stimulating directly different subsets of cortical neurons and recording the immediatereaction of the rest of the brain. Based onmeasurements performed in sleeping subjects(Massimini et al., 2005, 2007), we argue that thismethod represents an effective way to appreciate,at a general level, to what extent different regionsof the thalamocortical system can interact globally(
) to produce specific responses (
). Thus, instead of asking the subjects towilfully perform different motor or cognitivetasks, we directly ‘‘ask’’ (with TMS) their thalamocortical system to enter different neural statesand we assess (with hd-EEG) to what extent thesestates are integrated and specific. While thisapproach is not meant to tell whether a subjectis actually conscious or not, it may represent aprincipled way to objectively weigh a brain’scapacity for conscious experience.
Theoretical guidelines: the integrated informationtheory of consciousness
The IITC takes its start from phenomenology and,by making a critical use of thought experiments,argues that subjective experience
integratedinformation. Therefore, according to the IITC,any physical system will have subjective experience to the extent that it is capable of integratinginformation. In this view, experience, i.e. information integration, is a fundamental quantity that is,in principle, measurable, just as mass or energy is.Information and integration are, on the otherhand, the very essence of subjective experience.Classically, information is the reduction of uncertainty among alternatives: when a coin falls onone of its two sides, it provides 1 bit of information, whereas a die falling on one of sixfaces provides
2.6 bits. But then having anyconscious experience, even one of pure darkness,must be extraordinarily informative, because itrules out countless other experiences instead(think of all the frames of every possible movie).In other words, having any experience is likethrowing a die with a trillion faces and identifyingwhich number came up. On the other hand, everyexperience is an integrated whole that cannot besubdivided into independent components. Forexample, with an intact brain you cannot experience the left half of the visual field independentlyof the right half, or visual shapes independently of their colour. In other words, the die of experienceis a single one; throwing multiple dice andcombining the numbers will not help.If the capacity for consciousness corresponds tothe capacity to integrate information, then aphysical system should be able to generateconsciousness to the extent that it can discriminateamong a large number of available states (
), yet it cannot be decomposed into acollection of causally independent subsystems(
). How can one identify such anintegrated system, and how can one measure itsrepertoire of available states? To measure therepertoire of different states that are available to asystem, one can use the entropy function, but thisway of measuring information is completelyinsensitive to whether the information is integrated. Thus, measuring entropy would not allowus to distinguish between one million photodiodeswith a repertoire of two states each, and a singleintegrated system with a repertoire of 2
states. To measure information integration, it isessential to know whether a set of elementsconstitutes a causally integrated system, or theycan be broken down into a number of independent or quasi-independent subsets among whichno information can be integrated.Indeed, the theory claims that the level of consciousness of a physical system is related to therepertoire of different states (
) thatcan be discriminated by the system as a whole(
). Thus, a measure of integratedinformation, called phi (
), has been proposedin order to quantify the information generated

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