The wakeful brain can easily access and coordinate a large repertoire of different states—dynamics suggestive of “criticality.” Anesthesia causes loss of criticality at the level of electroencephalogram waveforms, but the criticality of brain network connectivity is less well studied. The authors hypothesized that propofol anesthesia is associated with abrupt and divergent changes in brain network connectivity for different frequencies and time scales—characteristic of a phase transition, a signature of loss of criticality.
As part of a previously reported study, 16 volunteers were given propofol in slowly increasing brain concentrations, and their behavioral responsiveness was assessed. The network dynamics from 31-channel electroencephalogram data were calculated from 1 to 20 Hz using four phase and envelope amplitude–based functional connectivity metrics that covered a wide range of time scales from milliseconds to minutes. The authors calculated network global efficiency, clustering coefficient, and statistical complexity (using the Jensen–Shannon divergence) for each functional connectivity metric and compared their findings with those from an in silico Kuramoto network model.
The transition to anesthesia was associated with critical slowing and then abrupt profound decreases in global network efficiency of 2 Hz power envelope metrics (from mean ± SD of 0.64 ± 0.15 to 0.29 ± 0.28 absolute value, P < 0.001, for medium; and from 0.47 ± 0.13 to 0.24 ± 0.21, P < 0.001, for long time scales) but with an increase in global network efficiency for 10 Hz weighted phase lag index (from 0.30 ± 0.20 to 0.72 ± 0.06, P < 0.001). Network complexity decreased for both the 10 Hz hypersynchronous (0.44 ± 0.13 to 0.23 ± 0.08, P < 0.001), and the 2 Hz asynchronous (0.73 ± 0.08 to 0.40 ± 0.13, P < 0.001) network states. These patterns of network coupling were consistent with those of the Kuramoto model of an order–disorder phase transition.
Around loss of behavioral responsiveness, a small increase in propofol concentrations caused a collapse of long time scale power envelope connectivity and an increase in 10 Hz phase-based connectivity—suggestive of a brain network phase transition.
- Changes in levels of consciousness are closely linked to anesthetics-induced dynamic alterations in functional connectivity of the central nervous system
- Propofol induces consistent global and regional decreases in functional brain connectivity when measured over the time scale of seconds to tens of seconds
- The question of how propofol affects neuronal network dynamics during both shorter (milliseconds) and longer (minutes) periods is incompletely explored
- Temporospatial electroencephalographic analysis of brain network dynamics over a wide range of frequencies and time scales in 16 volunteers receiving slowly increasing concentrations of propofol revealed that transition to unresponsiveness was associated with a sudden rise in alpha frequency network phase synchrony anteriorly, but also a transient surge and then loss of network coupling over long (tens of seconds) time scales
- Deep anesthesia was characterized by alpha waveform hypersynchrony and slow-wave power envelope dissynchrony across the whole cortex
- These observations suggest that propofol anesthesia is associated with a constellation of changes in network connectivity across frequencies and time scales that are signatures of sharp and sudden transitions in the behavior of networks