State-dependent, frequency-specific modulation of electrocortical traveling waves by anesthesia

Abstract

Emerging evidence suggests that cortical activity is organized in traveling waves that coordinate neural activity across space and time. How anesthesia alters these waves remains underexplored. We recently showed that cortical activity undergoes spontaneous state transitions at steady-state anesthetic concentrations including a paradoxical state exhibiting awake-like spectral properties during deep anesthesia. Here, we investigated traveling wave dynamics across spontaneous cortical states using hemispheric electrocorticography in rats anesthetized with desflurane at inhaled concentrations of 6, 4, 2, and 0%. Compared with the awake state, delta-band traveling waves in cortical states predominantly associated with 4-6% desflurane were more frequent and exhibited more stereotyped propagation patterns, characterized by a greater prevalence of planar waves and a corresponding reduction in source/sink wave patterns. The occurrence rate and pattern complexity of theta- and gamma-band waves remained largely unchanged, whereas the propagation direction of planar waves became more variable. Feedforward-feedback organization was also altered: compared with the awake state, the feedback-dominance of theta-band diminished, and the feed-forward dominance of gamma-band was attenuated. Despite occurring predominantly in deep anesthesia associated with behavioral unresponsiveness, traveling-wave dynamics of the paradoxical state exhibited partial, frequency-dependent shifts toward those observed in the awake state. These findings demonstrate that spontaneous cortical states under anesthesia are associated with frequency-dependent reorganization of cortical traveling waves and identify the paradoxical state as a distinct dynamical regime of deep anesthesia. Significance StatementAnesthesia is commonly thought to alter cortical dynamics progressively with increasing anesthetic depth, yet cortical activity can transition spontaneously between distinct states even at constant anesthetic concentrations. Here, we show that cortical states spectrally derived from the electrocorticogram of rats are associated with distinct frequency-specific organization of cortical traveling waves, revealing spatiotemporal dynamics beyond conventional spectral measures. Notably, a paradoxical state, occurred predominantly in deep anesthesia associated with behavioral unresponsiveness, exhibited traveling-wave dynamics that approached those observed during wakefulness. These findings demonstrate that cortical traveling-wave organization changes dynamically with brain state rather than anesthetic concentration alone. They suggest that structured cortical dynamics can emerge during deep anesthesia, providing new insights into large-scale cortical dynamics associated with anesthetic modulation of consciousness.