Theta and gamma rhythms coordinate large cell assemblies during locomotion. Their spread across temporal and spatial scales makes them challenging to observe. Additionally, the metabolic cost of these oscillations and their contribution to neuroimaging signals remains elusive. To finely characterize neurovascular interactions in running rats, we monitored brain hemodynamics with functional ultrasound and hippocampal local field potentials in running rats. Theta rhythm and running speed were strongly coupled to brain hemodynamics in multiple structures, with delays ranging from 0.8 seconds to 1.8 seconds. Surprisingly, hemodynamics was also strongly modulated across trials within the same recording session: cortical hemodynamics sharply decreased after 5-10 runs, while hippocampal hemodynamics strongly and linearly potentiated, particularly in the CA regions. This effect occurred while running speed and theta activity remained constant, and was accompanied by increased power in hippocampal high-frequency oscillations (100-150 Hz). Our findings reveal distinct vascular subnetworks modulated across fast and slow timescales and suggest strong adaptation processes despite stereotyped behavior.
IntroductionFrom the early days of electroencephalography (EEG), brain rhythms have been observed in a wide range of models and used as specific markers to characterize specific behaviors such as locomotion, sleep states, attention or cognitive control 1,2 . Neural oscillations support timely communication between coherent distant brain areas by providing windows of opportunity for efficient spike synchrony 3,4 and their disruption often is a hallmark of pathological conditions like epilepsy, schizophrenia, or Parkinson's disease 5 . Over the past decade, studies have reported that numerous brain rhythms are global processes that are not stationary, but instead circulate across brain regions. During locomotion in rodents, theta waves travel along the septotemporal axis of the hippocampus 6,7 , slow waves during NREM sleep travel from anterior towards posterior sites 8 and sleep spindles in humans rotate along a temporal, parietal and frontal cortical sites 9 . Because it is challenging to capture neural activity globally, this poses a problem from an experimental standpoint that high-density recordings can only partially solve, let alone the intrinsic caveats of electrophysiology.Theta rhythm (6-12 Hz) is extensively studied in behavioral neuroscience, because it is a fundamental model to understand neural synchronization during complex behavior. It is observable in many brain structures (hippocampus, entorhinal cortex, subiculum, striatum and thalamus) and species (bats, cats, rabbits, dogs, rodents, monkeys) 10 when an animal engages in walking, running, whisking and foraging behaviors or enters rapid-eye-movement sleep 11 . Among the multiple functions attributed to theta rhythm, it is critical for sensorimotor integration 12 , contextual information encoding 13 , hippocampal-cortical communication 14 and memory consolidation...