Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function?

Abstract

Spontaneous brain activity has recently received increasing interest in the neuroimaging community. However, the value of resting-state studies to a better understanding of brain-behavior relationships has been challenged. That altered states of consciousness are a privileged way to study the relationships between spontaneous brain activity and behavior is proposed, and common resting-state brain activity features observed in various states of altered consciousness are reviewed. Early positron emission tomography studies showed that states of extremely low or high brain activity are often associated with unconsciousness. However, this relationship is not absolute, and the precise link between global brain metabolism and awareness remains yet difficult to assert. In contrast, voxel-based analyses identified a systematic impairment of associative frontoparieto-cingulate areas in altered states of consciousness, such as sleep, anesthesia, coma, vegetative state, epileptic loss of consciousness, and somnambulism. In parallel, recent functional magnetic resonance imaging studies have identified structured patterns of slow neuronal oscillations in the resting human brain. Similar coherent blood oxygen level-dependent (BOLD) systemwide patterns can also be found, in particular in the default-mode network, in several states of unconsciousness, such as coma, anesthesia, and slow-wave sleep. The latter results suggest that slow coherent spontaneous BOLD fluctuations cannot be exclusively a reflection of conscious mental activity, but may reflect default brain connectivity shaping brain areas of most likely interactions in a way that transcends levels of consciousness, and whose functional significance remains largely in the dark.

FIGURE 1

Relationships between global brain metabolism and awareness. The link between global brain energy consumption and awareness is complex. Evidence exists that both states of extremely low and extremely high global brain metabolism are associated with small amounts of awareness. An intermediate level of brain metabolism, corresponding to a proper balance between inhibitory and excitatory neural activity, seems to be necessary to allow the genesis of awareness.

FIGURE 2

(Left) Consciousness has two main components: arousal, or the level of consciousness, and awareness, corresponding to the contents of consciousness per se. Arousal and awareness are usually positively correlated. However, they involve different brain structures. Arousal involves the activity of subcortical structures encompassing brain-stem reticular formation, hypothalamus, and basal forebrain. Awareness is related to the activity of a widespread set of frontoparietal associative areas, both on the convexity and on the midline. (Right) Awareness can in turn be divided into two main components: self and external awareness. In healthy volunteers, self- and external awareness are usually negatively correlated. Similarly, the frontoparietal awareness network can in turn be divided into two sub-systems, involved in self-and external awareness. Self-awareness networks encompass the posterior cingulate/precuneal cortices, medial frontal cortex, and bilateral temporoparietal junctions. The external awareness network encompasses lateral frontal and parietal cortices. In healthy volunteers, self- and external awareness networks usually show an anticorrelated pattern of activity.

FIGURE 3

Spontaneous anticorrelations between self- and external awareness networks in the conscious resting state, as observed in an individual volunteer. (Left) Areas correlated (above) and anticor-related (below) with the blood oxygen level–dependent (BOLD) time course of a seed voxel located in the posterior cingulate/precuneus. (Right) Plot of the BOLD time courses of posterior cingulate/precuneus (PCC, red/gray line) and of middle frontal gyrus (MFG, blue/dark line) in the same volunteer. As previously reported, anticorrelations between these area time courses occur in slow frequencies with a period below 0.1 Hz. (In color in Annals online.)

FIGURE 4

Preserved coherent blood oxygen level–dependent (BOLD) oscillations in the default network persist in three documented states of unawareness. Brain areas showing correlations with a seed voxel in the posterior cingulate cortex, after correction for spurious variance as described in Reference 91. From the left to the right, results of 12 volunteers' random-effect analysis, from an individual sleeping volunteer scanned during sleep stage 2 (from Ref. 68), from a patient in coma due to a nontraumatic origin, and anaesthetized monkey data (reproduced by permission from Vincent et al.91). Sleep and coma patients were masked inclusively with healthy volunteers' results to check for spatial consistency of the resting-state connectivity patterns.