Adaptive modulation of brain hemodynamics across stereotyped running episodes

Antoine Bergel (), Elodie Tiran, Thomas Deffieux, Charlie Demené, Mickaël Tanter () and Ivan Cohen ()
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Antoine Bergel: Sorbonne Université, CNRS, INSERM, Institut de Biologie Paris Seine-Neuroscience
Elodie Tiran: Physique pour la Médecine Paris, INSERM U1273, ESPCI Paris, CNRS FRE 2031, PSL Université Recherche
Thomas Deffieux: Physique pour la Médecine Paris, INSERM U1273, ESPCI Paris, CNRS FRE 2031, PSL Université Recherche
Charlie Demené: Physique pour la Médecine Paris, INSERM U1273, ESPCI Paris, CNRS FRE 2031, PSL Université Recherche
Mickaël Tanter: Physique pour la Médecine Paris, INSERM U1273, ESPCI Paris, CNRS FRE 2031, PSL Université Recherche
Ivan Cohen: Sorbonne Université, CNRS, INSERM, Institut de Biologie Paris Seine-Neuroscience

Nature Communications, 2020, vol. 11, issue 1, 1-19

Abstract: Abstract During locomotion, theta and gamma rhythms are essential to ensure timely communication between brain structures. However, their metabolic cost and contribution to neuroimaging signals remain elusive. To finely characterize neurovascular interactions during locomotion, we simultaneously recorded mesoscale brain hemodynamics using functional ultrasound (fUS) and local field potentials (LFP) in numerous brain structures of freely-running overtrained rats. Locomotion events were reliably followed by a surge in blood flow in a sequence involving the retrosplenial cortex, dorsal thalamus, dentate gyrus and CA regions successively, with delays ranging from 0.8 to 1.6 seconds after peak speed. Conversely, primary motor cortex was suppressed and subsequently recruited during reward uptake. Surprisingly, brain hemodynamics were strongly modulated across trials within the same recording session; cortical blood flow sharply decreased after 10–20 runs, while hippocampal responses strongly and linearly increased, particularly in the CA regions. This effect occurred while running speed and theta activity remained constant and was accompanied by an increase in the power of hippocampal, but not cortical, high-frequency oscillations (100–150 Hz). Our findings reveal distinct vascular subnetworks modulated across fast and slow timescales and suggest strong hemodynamic adaptation, despite the repetition of a stereotyped behavior.

Date: 2020
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DOI: 10.1038/s41467-020-19948-7

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