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Authors & Affiliations
Antoine Bergel, Marta Matei, Sophie Pezet, Adrien Peyrache, Karim Benchenane, Mickaël Tanter
Abstract
Episodic memories become gradually independent from the hippocampus and progressively consolidate in the neocortex. During sleep and rest periods, neuronal traces are reactivated at the time of hippocampal sharp-wave ripples (SWRs) thought to mediate memory consolidation. Though SWRs have been widely studied within the hippocampus, the ongoing activity within the rest of the brain remains elusive, because technically challenging: electrophysiology cannot easily resolve the whole brain and optical recording techniques have limited access to deep tissue. In a 2012 study, Logothetis and colleagues used fMRI to demonstrate that, during SWRs, hippocampal-cortex interactions occur over a background of subcortical silence. Here we used the emerging modality functional ultrasound (fUS) imaging to monitor brain activity during NREM sleep in rats, over a series of coronal and sagittal slices, spanning more than 2/3 of the cerebrum, and revealed the precise spatiotemporal hemodynamics around SWRs in both cortical and subcortical structures. We confirm that SWRs are consistently followed by robust vascular activations in the dorsal hippocampus and association cortices, particularly in the retrosplenial and prefrontal cortices, peaking 1.5 to 2 seconds after peak ripple time, consistent with neurovascular coupling delays. We did not observe significant activations in subcortical structures. We also demonstrate different cortical coupling for longest ripples compared to faster ones, suggesting that different ripple types may have different cortical correlates. Taken together, our approach provides new insights into the large-scale dynamics of hippocampal-cortex interactions at unprecedented resolution.