Pyramidal Neurons Are "Neurogenic Hubs" in the Neurovascular Coupling Response to Whisker Stimulation

Clotilde Lecrux, Xavier Toussay, Ara Kocharyan, Priscilla Fernandes, Sujay Neupane, Maxime Levesque, Fabrice Plaisier, Amir Shmuel, Bruno Cauli, Edith Hamel*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

The whisker-to-barrel cortex is widely used to study neurovascular coupling, but the cellular basis that underlies the perfusion changes is still largely unknown. Here, we identified neurons recruited by whisker stimulation in the rat somatosensory cortex using double immunohistochemistry for c-Fos and markers of glutamatergic and GABAergic neurons, and investigated in vivo their contribution along with that of astrocytes in the evoked perfusion response. Whisker stimulation elicited cerebral blood flow (CBF) increases concomitantly with c-Fos upregulation in pyramidal cells that coexpressed cyclooxygenase-2 (COX-2) and GABA interneurons that coexpressed vasoactive intestinal polypeptide and/or choline acetyltransferase, but not somatostatin or parvalbumin. The evoked CBF response was decreased by blockade of NMDA (MK-801, -37%), group I metabotropic glutamate (MPEP + LY367385, -40%), and GABA-A (picrotoxin, -31%) receptors, but not by GABA-B, VIP, or muscarinic receptor antagonism. Picrotoxin decreased stimulus-induced somatosensory evoked potentials and CBF responses. Combined blockade of GABA-A and NMDA receptors yielded an additive decreasing effect (-61%) of the evoked CBF compared with each antagonist alone, demonstrating cooperation of both excitatory and inhibitory systems in the hyperemic response. Blockade of prostanoid synthesis by inhibiting COX-2 (indomethacin, NS-398), expressed by similar to 40% of pyramidal cells but not by astrocytes, impaired the CBF response (-50%). The hyperemic response was also reduced (-40%) after inhibition of astroglial oxidative metabolism or epoxyeicosatrienoic acids synthesis. These results demonstrate that changes in pyramidal cell activity, sculpted by specific types of inhibitory GABA interneurons, drive the CBF response to whisker stimulation and, further, that metabolically active astrocytes are also required.

Original languageEnglish
Pages (from-to)9836-9847
Number of pages12
JournalJournal of Neuroscience
Volume31
Issue number27
DOIs
Publication statusPublished - 6 Jul 2011

Keywords

  • PRIMARY SOMATOSENSORY CORTEX
  • CEREBRAL-BLOOD-FLOW
  • RAT BARREL CORTEX
  • SYNCHRONIZED GAMMA-OSCILLATIONS
  • OPTICAL IMAGING SPECTROSCOPY
  • CORTICAL GABA INTERNEURONS
  • LASER-DOPPLER FLOWMETRY
  • C-FOS EXPRESSION
  • IN-VIVO
  • GABAERGIC NEURONS

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