Sensory-Related Neural Activity Regulates the Structure of Vascular Networks in the Cerebral Cortex

Abstract

SUMMARY Neurovascular interactions are essential for proper brain function. While the effect of neural activity on cerebral blood flow has been extensively studied, whether neural activity influences vascular patterning remains elusive. Here, we demonstrate that neural activity promotes the formation of vascular networks in the early postnatal mouse barrel cortex. Using a combination of genetics, imaging, and computational tools to allow simultaneous analysis of neuronal and vascular components, we found that vascular density and branching were decreased in the barrel cortex when sensory input was reduced by either a complete deafferentation, a genetic impairment of neurotransmitter release at thalamocortical synapses, or a selective reduction of sensory-related neural activity by whisker plucking. In contrast, enhancement of neural activity by whisker stimulation led to an increase in vascular density and branching. The finding that neural activity is necessary and sufficient to trigger alterations of vascular networks reveals a novel feature of neurovascular interactions.

Stochastic electrotransport selectively enhances the transport of highly electromobile molecules

“…Our preliminary data show that distinct brain regions exhibited different cell body density and nuclei-vascular distance profiles. Such quantitative analysis may reveal important structural or pathological features of the vascular network or cell-vascular interactions in normal or diseased brain tissues (41)(42)(43)(44). Together, these results demonstrate that stochastic electrotransport may be useful for rapid and quantitative 3D phenotyping of organ-scale biological systems.…”

Cellular diversity of the somatosensory cortical map plasticity

“…These anti-angiogenic effects were associated with hypoxic conditions in the corresponding overstimulated brain regions, which in turn was accompanied dendritic spine loss. A separate study (Lacoste et al, 2014) employed both enhanced and decreased whisker experience, and found that blood vessel patterning in barrel cortex was modulated as a result: vascular density and branching were diminished in response to whisker deprivation whereas the same metrics were enhanced upon whisker stimulation. These findings indicate that the organization of the neurovascular bed is modulated in the wake of sensory experience, and suggest that brain oxygen levels (which are a derivative of brain vascularization) can in fact form a limiting factor to synaptic plasticity.…”

“…PDGF-BB-mediated induction of chemotaxis and mitogenesis in vascular smooth muscle cells requires PLAT, linking PDGF-B to yet another vasculature modulator (Herbert et al, 1997). Because these genes are expressed in an activitydependent manner (based on (Vallès et al, 2011)), pathways such as these could well orchestrate blood vessel patterning to suit the needs of neuronal circuits (Lacoste et al, 2014;Whiteus et al, 2014).…”

L’activité neuronale influence le développement des vaisseaux sanguins du cerveau

“…Ce n'est que très récemment que la contribution de l'activité neuronale au développement cérébrovasculaire a été démontrée, à la suite de notre étude dans le laboratoire de Chenghua Gu à l'Université Harvard [11]. Il est important d'évoquer la parution, quelques mois avant notre article, d'une étude rapportant l'effet néfaste de l'hyperactivité neuronale sur la maturation des vaisseaux cérébraux [12].…”