Hippocampal-like network dynamics underlie avian sharp wave-ripples

Abstract

Sharp wave ripples (SWR) represent one of the most synchronous population patterns in the mammalian brain. Although SWRs are highly conserved throughout mammalian evolution, the existence of SWRs in non-mammalian species remains controversial. We reexamined the existence of avian SWRs by recording the brain activity during sleep and under anesthesia in two species of birds, the zebra finch and the chicken. Electrophysiological recordings using silicon probes implanted in the avian telencephalon revealed highly dynamic switching between high and low delta phases during sleep. High delta phases were composed of large-amplitude, negative deflections (sharp waves) that coincided with a high frequency oscillation (ripple). Correlation analysis revealed that these events were highly synchronous and spanned a large anatomical range of the avian telencephalon. Finally, detailed spike analysis revealed that an increase in the population spiking activity coincided with the occurrence of SWRs, that this spiking activity occurred in specific sequences of spike patterns locked to the SWRs, and that the mean population spiking activity peaked prior to the trough of the negative deflection. These results provide the first evidence of avian SWRs during natural sleep and under anesthesia, and suggest that the evolutionary origin of SWR activity may precede the mammalian-sauropsid bifurcation.