Astrocyte morphology is confined by cortical functional boundaries in mammals ranging from mice to human.

Raya Eilam,Rina Aharoni,Rafael Malach,Ruth Arnon

doi:10.7554/elife.15915

Abstract

Cortical blood flow can be modulated by local activity across a range of species; from barrel-specific blood flow in the rodent somatosensory cortex to the human cortex, where BOLD-fMRI reveals numerous functional borders. However, it appears that the distribution of blood capillaries largely ignores these functional boundaries. Here we report that, by contrast, astrocytes, a major player in blood-flow control, show a striking morphological sensitivity to functional borders. Specifically, we show that astrocyte processes are structurally confined by barrel boundaries in the mouse, by the border of primary auditory cortex in the rat and by layers IIIa/b and Cytochrome Oxidase (CO)-blobs boundaries in the human primary visual cortex. Thus, astrocytes which are critical elements in neuro-hemodynamic coupling show a significant anatomical segregation along functional boundaries across different mammalian species. These results may open a new anatomical marker for delineating functional borders across species, including post-mortem human brains.

Highlights

The cerebral cortex has a remarkable capacity to regulate its own blood supply according to local neuronal activity demands (Buxton and Frank, 1997)
Our examination of barrel field tissue was based on 154/146 measurements conducted in 4 sections in five left hemispheres of five mice and on 56/54 measurements calculatedin two additional left hemispheres
Our results reveal a novel structural manifestation of cortical architecture, reflected in the tendency of astrocyte processes to be anatomically confined by functional borders

Summary

Introduction

The cerebral cortex has a remarkable capacity to regulate its own blood supply according to local neuronal activity demands (Buxton and Frank, 1997) This mechanism is of great interest, since it is the basis of optical imaging of intrinsic signals (Vanzetta and Grinvald, 1999) as well as BOLD-fMRI imaging (Logothetis et al, 2001). Given the tight coupling between columnar neuronal activation and blood flow, one could envision that the cortical vascular architecture should show anatomical shaping according to these boundaries. Such structural confinements by columnar boundaries were previously demonstrated in the dendritic and axonal arbors of barrel field neurons.

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