J.-P. Changeux and C. M. Michel The Functional Microstates of the Brain

Figure 17.2 Assessment of the functional microstates of the brain. (a) Synchronous activity of a large number of neurons in a given cortical region leads to a sum electric field that spreads throughout the brain and reaches the cortical surface. By placing a large number of electrodes on the scalp surface (here: 128), the instantaneous electric field can be recorded directly and displayed as a scalp potential map in 3D or as a planar projection. (b) 10 seconds of spontaneous EEG recorded from 128 electrodes. Below some selected traces, a series of scalp potential maps is shown (note than only a subsampling of the total 5000 maps is shown). The 9 maps at the bottom are the result of a k-means spatial cluster analysis that determined the most dominant map configurations present in the data. The bar below the map series indicates the periods during which each of these maps was present. The striking finding is that the electric activity can be divided into time segments of around 80-150 ms duration that are each characterized by a stable map configuration. It is believed that each of these periods represents a functional microstate of the brain, that is, an "atom of thought." (c) Brain electric responses evoked by a stimulus (a word in this example) simultaneously recorded from 128 scalp electrodes. The evoked potentials for the 600 ms post-stimulus are shown as overlaid traces. Below them, the map series during this period is shown (again only a subsample). The spatial cluster analysis revealed that 7 maps best explain the whole data set (shown on the bottom). The bar illustrates the period during which each of these 7 maps was present. Again, segments of stable map configuration, lasting between 80-150 ms are found. It is assumed that each of these evoked functional microstates represents a given information-processing step.

particular "steps" or "contents" of information processing; that is, they are the basic building blocks of the content of consciousness: "atoms of thoughts" (Koukkou and Lehmann 1987; Lehmann 1992) or "mental objects" (Changeux 1983), therefore the term "functional microstate" (note that "micro" here refers to the temporal not the spatial scale). According to this interpretation, what William James (1890) referred to as the "stream of consciousness" might not be continuous, but a sequence of separable, distinct, microstates that implement different mental contents. In keeping with the neuronal workspace model, we wish to suggest the hypothesis that the experimental functional microstates of the brain implement the postulated spontaneous or evoked coherent activation of workspace neurons. In other words, they would be electrophysiological correlates of a process of global "conscious" integration at the brain-scale level. They might also be viewed as implementing the proposal of Crick and Koch (2003) that, in the case of motion, perception consists of discrete processing epochs or "snapshots" as well as Oliver Sacks's clinical observations (2004) of patients who see movement as a succession of "stills" during migraine episodes.

These functional microstates have been systematically recorded in human subjects and analyzed in different "mental" conditions offering clues about the duration of what might be viewed as basic building blocks ofthe content of consciousness. A recent comprehensive analysis of496 subjects between the age of 6 and 80 years revealed mean microstate durations of 80-150 ms (Koenig et al. 2002), confirming earlier studies with a smaller number of subjects (Wackermann et al. 1993; Lehmann et al. 1998). The duration decreases slowly during childhood and then stabilizes in adulthood (Koenig et al. 2002). According to Lehmann et al. (1998) these microstates would represent the elementary psychophysiological units of cognition and emotion. For instance, in an experiment where subjects were asked to recall spontaneous, conscious experiences after the presentation of a prompt signal, the reports could successfully be classified into imagery and abstract thoughts on the basis of the topography of the microstate just preceding the prompt. The duration of these microstates was on average 121 ms, indicating that approximately this duration of near-stable brain activity suffices for a conscious experience. Interestingly, cognitive event-related potential components, such as the CNV, the P300, or the N400, are characterized by periods of stable map topographies of approximately this duration (e.g., Michel etal. 1992; Pegnaetal. 1997; Khateb etal. 2000,2003; Schnideret al. 2002; Murray et al. 2004). Moreover, the more effortful the task process, the longer was the duration ofthe corresponding cognitive microstates (Pegna et al. 1997; Khateb etal. 2000). Other evidence has led to similar recordings of activity parcellation into sequential episodes of around 100 ms, making the functional microstates plausible candidates for the electrophysiological manifestation of these global episodes of conscious experience. For example, sequentially presented stimuli are not perceived as separate when they follow each other within less than 80 ms (Efron 1970). Masking a stimulus is efficient when presented with a latency of less than 100 ms (Libet 1981; Dehaene et al. 2003; Sergent and Dehaene 2004). Other studies have reported similar durations for episodes of synchronous thalamo-cortical activity (Llinas and Ribary 1998), sequences of alpha bursts (Williamson et al. 1996), or of EPSP-IPSP in mammalian forebrain neurons (Purpura 1972; review in John 2002). Thus, the functional microstates, expressed as periods of stable scalp electrical potential topographies, may be viewed as neural implementations of the elementary building blocks of consciousness content. In line with this view is the recent demonstration of shortening of certain microstates in schizophrenics, which could functionally be interpreted as a precocious termination of information processing in certain classes of mental operations due to degraded cooperativity of neural assemblies in these patients (Lehmann et al. 2005).

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