Abstract
The spatial-temporal sequence of cerebral blood flow (CBF), cerebral blood volume (CBV) and blood velocity changes triggered by neuronal activation is critical for understanding functional brain imaging. This sequence follows a stereotypic pattern of changes across different zones of the vasculature in the olfactory bulb, the first relay of olfaction. However, in the cerebral cortex, where most human brain mapping studies are performed, the timing of activity evoked vascular events remains controversial. Here we utilized a single whisker stimulation model to map out functional hyperemia along vascular arbours from layer II/III to the surface of primary somatosensory cortex, in anesthetized and awake Thy1-GCaMP6 mice. We demonstrate that sensory stimulation triggers an increase in blood velocity within the mid-capillary bed and a dilation of upstream large capillaries, and the penetrating and pial arterioles. We report that under physiological stimulation, response onset times are highly variable across compartments of different vascular arbours. Furthermore, generating transfer functions (TFs) between neuronal Ca2+ and vascular dynamics across different brain states demonstrates that anesthesia decelerates neurovascular coupling (NVC). This spatial-temporal pattern of vascular events demonstrates functional diversity not only between different brain regions but also at the level of different vascular arbours within supragranular layers of the cerebral cortex.
Highlights
The spatial-temporal sequence of cerebral blood flow (CBF), cerebral blood volume (CBV) and blood velocity changes triggered by neuronal activation is critical for understanding functional brain imaging
In the specialized olfactory bulb (OB) glomerular model, synaptic activation is concentrated around the mid-capillary bed, constituted by an extremely dense network of capillaries outlined by long thin-strand pericytes
We first set out to examine the dynamics of functional hyperemia across the vascular arbor of ketamine–medetomidine anesthetized mice
Summary
The spatial-temporal sequence of cerebral blood flow (CBF), cerebral blood volume (CBV) and blood velocity changes triggered by neuronal activation is critical for understanding functional brain imaging. Increasing evidence suggests that the “transitional segment”, “pre-capillary arteriole” or “secondary functional unit” (as we named in the OB) must be considered a specific functional compartment, distinct from both the downstream capillary bed and the upstream arteriole This compartmentalized distinction is highlighted by recent anatomical studies characterizing the presence and variability in the morphology of smooth-muscle cell and pericyte sub-types and their expression of the contractile protein α-SMA, exhibiting variable length and branch order coverage after the penetrating arteriole between different vascular arbors[8,9,10], thereby raising the question of whether similar branch order variability could exist in the onset timings of compartment specific vasodilation. We utilized a single whisker deflection paradigm and neuronal Ca2+ signals in Thy1-GCaMP6 mice to reinvestigate the degree of stereotypy or diversity of the sequence of diameter and velocity dynamics along layer 2/3 (L2/3) vascular arbors in relation to sensory-evoked neuronal activity
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