Sensory-related neural activity regulates the structure of vascular networks in the cerebral cortex

Neuron. 2014 Sep 3;83(5):1117-30. doi: 10.1016/j.neuron.2014.07.034. Epub 2014 Aug 21.

Abstract

Neurovascular interactions are essential for proper brain function. While the effect of neural activity on cerebral blood flow has been extensively studied, whether or not 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 an important feature of neurovascular interactions.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Afferent Pathways / physiology*
  • Age Factors
  • Animals
  • Animals, Newborn
  • Cell Proliferation
  • Cerebral Cortex / cytology*
  • Cerebral Cortex / physiology*
  • Cerebrovascular Circulation / physiology*
  • GTP-Binding Proteins / genetics
  • GTP-Binding Proteins / metabolism
  • Gene Expression Regulation, Developmental / genetics
  • In Vitro Techniques
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Mice
  • Mice, Transgenic
  • Phosphopyruvate Hydratase / metabolism
  • Physical Stimulation
  • Receptor, TIE-2 / genetics
  • Receptor, TIE-2 / metabolism
  • Sensory Receptor Cells / physiology*
  • Vibrissae / injuries
  • Vibrissae / physiology*
  • rab3 GTP-Binding Proteins / genetics

Substances

  • Luminescent Proteins
  • Rims1 protein, mouse
  • Receptor, TIE-2
  • Tek protein, mouse
  • GTP-Binding Proteins
  • Rim2 protein, mouse
  • rab3 GTP-Binding Proteins
  • Phosphopyruvate Hydratase