The signature of consciousness in resting-state brain activity.

I've done a number of posts on attentional or salience versus default mode long-range connectivity networks in our brains (for a review see my lecture.) They correspond roughly to supporting outward task oriented processes versus inward processes such as daydreaming or imagining. Activity in these networks is thought to be a marker of consciousness, but this idea conflicts with observations that long-range functional connectivities persist even after loss of consciousness caused by anesthesia, or in vegetative state patients. This post is to point to recent work by Dehaene and collaborators showing clear difference in the behavior of long-range networks in awake and anesthetized monkeys. Their abstract and statement of significance, followed by a movie showing whole brain connectivity patterns at different time points in the awake monkey.

Significance

What are the origins of resting-state functional connectivity patterns? One dominating view is that they index ongoing cognitive processes. However, this conclusion is in conflict with studies showing that long-range functional connectivity persists after loss of consciousness, possibly reflecting structural connectivity maps. In this work we respond to this question showing that in fact both sources have a clear and separable contribution to resting-state patterns. We show that under anesthesia, the dominating functional configurations have low information capacity and lack negative correlations. Importantly, they are rigid, tied to the anatomical map. Conversely, wakefulness is characterized by the dynamical exploration of a rich, flexible repertoire of functional configurations. These dynamical properties constitute a signature of consciousness.

Abstract

At rest, the brain is traversed by spontaneous functional connectivity patterns. Two hypotheses have been proposed for their origins: they may reflect a continuous stream of ongoing cognitive processes as well as random fluctuations shaped by a fixed anatomical connectivity matrix. Here we show that both sources contribute to the shaping of resting-state networks, yet with distinct contributions during consciousness and anesthesia. We measured dynamical functional connectivity with functional MRI during the resting state in awake and anesthetized monkeys. Under anesthesia, the more frequent functional connectivity patterns inherit the structure of anatomical connectivity, exhibit fewer small-world properties, and lack negative correlations. Conversely, wakefulness is characterized by the sequential exploration of a richer repertoire of functional configurations, often dissimilar to anatomical structure, and comprising positive and negative correlations among brain regions. These results reconcile theories of consciousness with observations of long-range correlation in the anesthetized brain and show that a rich functional dynamics might constitute a signature of consciousness, with potential clinical implications for the detection of awareness in anesthesia and brain-lesioned patients.

Dynamical connectivity matrix - red lines mark positive correlations, and blue lines mark negative correlations.