Parvalbumin interneuron activity drives fast inhibition-induced vasoconstriction followed by slow substance P-mediated vasodilation

The role of parvalbumin (PV) interneurons in vascular control is poorly understood. Here, we investigated the hemodynamic responses elicited by optogenetic stimulation of PV interneurons using electrophysiology, functional magnetic resonance imaging (fMRI), wide-field optical imaging (OIS), and phar...

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Published in:Proceedings of the National Academy of Sciences - PNAS 2023-05, Vol.120 (18), p.e2220777120-e2220777120
Main Authors: Vo, Thanh Tan, Im, Geun Ho, Han, Kayoung, Suh, Minah, Drew, Patrick J, Kim, Seong-Gi
Format: Article
Language:English
Subjects:
Anesthesia
Biological Sciences
Brain mapping
Electrophysiology
Functional magnetic resonance imaging
Hemodynamic responses
Interneurons
Interneurons - physiology
Magnetic resonance imaging
Neuroimaging
Neuronal-glial interactions
Neurons
Parvalbumin
Parvalbumins - metabolism
Sleep and wakefulness
Somatosensory cortex
Stimulation
Substance P
Substance P - metabolism
Substance P - pharmacology
Vasoconstriction
Vasodilation
Wakefulness
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Summary:The role of parvalbumin (PV) interneurons in vascular control is poorly understood. Here, we investigated the hemodynamic responses elicited by optogenetic stimulation of PV interneurons using electrophysiology, functional magnetic resonance imaging (fMRI), wide-field optical imaging (OIS), and pharmacological applications. As a control, forepaw stimulation was used. Stimulation of PV interneurons in the somatosensory cortex evoked a biphasic fMRI response in the photostimulation site and negative fMRI signals in projection regions. Activation of PV neurons engaged two separable neurovascular mechanisms in the stimulation site. First, an early vasoconstrictive response caused by the PV-driven inhibition is sensitive to the brain state affected by anesthesia or wakefulness. Second, a later ultraslow vasodilation lasting a minute is closely dependent on the sum of interneuron multiunit activities, but is not due to increased metabolism, neural or vascular rebound, or increased glial activity. The ultraslow response is mediated by neuropeptide substance P (SP) released from PV neurons under anesthesia, but disappears during wakefulness, suggesting that SP signaling is important for vascular regulation during sleep. Our findings provide a comprehensive perspective about the role of PV neurons in controlling the vascular response.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2220777120