Better explicating the strengths and shortcomings of these models will help refine projections and improve transparency in the years ahead.
Image credit: Witsawat.S.
Contributed by Donald W. Pfaff, May 13, 2014 (sent for review January 15, 2014)
Significance
How does the brain recover consciousness after significant perturbations such as anesthesia? The simplest answer is that as the anesthetic washes out, the brain follows a steady and monotonic path toward consciousness. We show that this simple intuition is incorrect. We varied the anesthetic concentration to parametrically control the magnitude of perturbation to brain dynamics while analyzing the characteristics of neuronal activity during recovery of consciousness. We find that, en route to consciousness, the brain passes through several discrete activity states. Although transitions between certain of these activity states occur spontaneously, transitions between others are not observed. Thus, the network formed by these state transitions gives rise to an ordered sequence of states that mediates recovery of consciousness.
Abstract
It is not clear how, after a large perturbation, the brain explores the vast space of potential neuronal activity states to recover those compatible with consciousness. Here, we analyze recovery from pharmacologically induced coma to show that neuronal activity en route to consciousness is confined to a low-dimensional subspace. In this subspace, neuronal activity forms discrete metastable states persistent on the scale of minutes. The network of transitions that links these metastable states is structured such that some states form hubs that connect groups of otherwise disconnected states. Although many paths through the network are possible, to ultimately enter the activity state compatible with consciousness, the brain must first pass through these hubs in an orderly fashion. This organization of metastable states, along with dramatic dimensionality reduction, significantly simplifies the task of sampling the parameter space to recover the state consistent with wakefulness on a physiologically relevant timescale.
Footnotes
↵1A.E.H. and D.P.C. contributed equally to this work.
- ↵2To whom correspondence may be addressed. E-mail: proekt{at}gmail.com or pfaff{at}rockefeller.edu.
Author contributions: A.E.H., D.P.C., D.W.P., and A.P. designed research; A.E.H., D.P.C., and A.P. performed research; A.E.H. and A.P. analyzed data; and A.E.H., D.P.C., D.W.P., and A.P. wrote the paper.
The authors declare no conflict of interest.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1408296111/-/DCSupplemental.
Freely available online through the PNAS open access option.
Discrete activity states en route to consciousness
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