Ramirez Villegas, Juan FISTA; Besserve, Michel; Murayama, Yusuke; Evrard, Henry C.; Oeltermann, Axel; Logothetis, Nikos K.
The hippocampus has a major role in encoding and consolidating long-term memories, and undergoes plastic changes during sleep1. These changes require precise homeostatic control by subcortical neuromodulatory structures2. The underlying mechanisms of this phenomenon, however, remain unknown. Here, using multi-structure recordings in macaque monkeys, we show that the brainstem transiently modulates hippocampal network events through phasic pontine waves known as pontogeniculooccipital waves (PGO waves). Two physiologically distinct types of PGO wave appear to occur sequentially, selectively influencing high-frequency ripples and low-frequency theta events, respectively. The two types of PGO wave are associated with opposite hippocampal spike-field coupling, prompting periods of high neural synchrony of neural populations during periods of ripple and theta instances. The coupling between PGO waves and ripples, classically associated with distinct sleep stages, supports the notion that a global coordination mechanism of hippocampal sleep dynamics by cholinergic pontine transients may promote systems and synaptic memory consolidation as well as synaptic homeostasis.
We thank O. Eschenko and M. Constantinou for providing feedback on earlier versions of this work, and J. Werner and M. Schnabel for technical support during the development of this study. This research was supported by the Max Planck Society.
Ramirez Villegas JF, Besserve M, Murayama Y, Evrard HC, Oeltermann A, Logothetis NK. Coupling of hippocampal theta and ripples with pontogeniculooccipital waves. Nature. 2021;589(7840):96-102. doi:10.1038/s41586-020-2914-4
Ramirez Villegas, J. F., Besserve, M., Murayama, Y., Evrard, H. C., Oeltermann, A., & Logothetis, N. K. (2021). Coupling of hippocampal theta and ripples with pontogeniculooccipital waves. Nature. Springer Nature. https://doi.org/10.1038/s41586-020-2914-4
Ramirez Villegas, Juan F, Michel Besserve, Yusuke Murayama, Henry C. Evrard, Axel Oeltermann, and Nikos K. Logothetis. “Coupling of Hippocampal Theta and Ripples with Pontogeniculooccipital Waves.” Nature. Springer Nature, 2021. https://doi.org/10.1038/s41586-020-2914-4.
J. F. Ramirez Villegas, M. Besserve, Y. Murayama, H. C. Evrard, A. Oeltermann, and N. K. Logothetis, “Coupling of hippocampal theta and ripples with pontogeniculooccipital waves,” Nature, vol. 589, no. 7840. Springer Nature, pp. 96–102, 2021.
Ramirez Villegas JF, Besserve M, Murayama Y, Evrard HC, Oeltermann A, Logothetis NK. 2021. Coupling of hippocampal theta and ripples with pontogeniculooccipital waves. Nature. 589(7840), 96–102.
Ramirez Villegas, Juan F., et al. “Coupling of Hippocampal Theta and Ripples with Pontogeniculooccipital Waves.” Nature, vol. 589, no. 7840, Springer Nature, 2021, pp. 96–102, doi:10.1038/s41586-020-2914-4.