Speed Vascular Patterns in the Spatial Navigation System

Abstract

The hippocampal formation is central to spatial navigation, hosting neurons that encode position, direction, and speed. Yet, the brain-wide vascular dynamics supporting these processes remain poorly understood, especially during naturalistic behaviors. Here, we adapted functional ultrasound (fUS) imaging to examine how cerebral blood volume (CBV) changes relate to behavioral parameters in freely moving rats. High-resolution imaging of hippocampal-parahippocampal regions during open-field exploration reveals strong correlations between CBV dynamics and animal speed, with distinct regional activation patterns and temporal delays. Lagged general linear modeling uncovers information flow from the thalamus to parahippocampal regions, including the medial entorhinal cortex, and to hippocampal subfields (dentate gyrus, CA1-CA3), consistent with a hierarchical processing framework. The analysis also links CBV with angular head speed and the dorsal thalamus. Decoding analyses show that CBV signals not only encode speed precisely but also capture spatial features like proximity to walls and corners, even when univariate analyses do not. This decoding remains robust across animals, underscoring the universality of speed encoding in vascular dynamics. We also identify slow CBV oscillations in the hippocampus aligned with minute-scale speed fluctuations, suggesting a neurovascular signature of exploratory behavior. These findings reveal a hemodynamic signature of speed representation in the navigation system, arising from energy demands in a continuous attractor network model for path integration, where population activity and synaptic currents increase quadratically with animal speed as both peak firing rates and neuronal recruitment scale linearly with animal speed. Moreover, they highlight functional ultrasound imaging as a powerful approach for probing the hemodynamic basis of navigation.