Signature of consciousness in the dynamics of resting-state brain activity

Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved December 4, 2014 (received for review September 19, 2014)

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.

Footnotes

1P.B., L.U., and J.D.S. contributed equally to this work.
2To whom correspondence may be addressed. Email: pablo.barttfeld@cea.fr, bechir.jarraya@cea.fr, orstanislas.dehaene@cea.fr.

Author contributions: B.J. and S.D. designed research; L.U. performed research; P.B., J.D.S., M.S., and S.D. analyzed data; and P.B., L.U., J.D.S., M.S., B.J., and S.D. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1418031112/-/DCSupplemental.