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Modification of oxygen consumption and blood flow in mouse somatosensory cortex by cell-type-specific neuronal activity.

ABSTRACT: Gamma activity arising from the interplay between pyramidal neurons and fast-spiking parvalbumin (PV) interneurons is an integral part of higher cognitive functions and is assumed to contribute significantly to brain metabolic responses. Cerebral metabolic rate of oxygen (CMRO₂) responses were evoked by optogenetic stimulation of cortical PV interneurons and pyramidal neurons. We found that CMRO₂ responses depended on neuronal activation, but not on the power of gamma activity induced by optogenetic stimulation. This implies that evoked gamma activity per se is not energy demanding. Optogenetic stimulation of PV interneurons during somatosensory stimulation reduced excitatory neuronal activity but did not potentiate O₂ consumption as previously hypothesized. In conclusion, our data suggest that activity-driven CMRO₂ responses depend on neuronal excitation rather than the cerebral rhythmic activity they induce. Excitation of both excitatory and inhibitory neurons requires energy, but inhibition of cortical excitatory neurons by interneurons does not potentiate activity-driven energy consumption.

SUBMITTER: Dahlqvist MK

PROVIDER: S-EPMC7786843 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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Modification of oxygen consumption and blood flow in mouse somatosensory cortex by cell-type-specific neuronal activity.

Dahlqvist Matilda K MK Thomsen Kirsten J KJ Postnov Dmitry D DD Lauritzen Martin J MJ

Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism 20191023 10

Gamma activity arising from the interplay between pyramidal neurons and fast-spiking parvalbumin (PV) interneurons is an integral part of higher cognitive functions and is assumed to contribute significantly to brain metabolic responses. Cerebral metabolic rate of oxygen (CMRO<sub>2</sub>) responses were evoked by optogenetic stimulation of cortical PV interneurons and pyramidal neurons. We found that CMRO<sub>2</sub> responses depended on neuronal activation, but not on the power of gamma activ ...[more]

PMID: 31645177

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Project description:Cocaine affects both cerebral blood vessels and neuronal activity in brain. Cocaine can also disrupt astrocytes, which modulate neurovascular coupling-a process that regulates cerebral hemodynamics in response to neuronal activation. However, separating neuronal and astrocytic effects from cocaine's direct vasoactive effects has been challenging, partially due to limitations of neuroimaging techniques able to differentiate vascular from neuronal and glial effects at high temporal and spatial resolutions. Here, we used a newly-developed multi-channel fluorescence and optical coherence Doppler microscope (fl-ODM) that allows for simultaneous measurements of neuronal and astrocytic activities (reflected by the intracellular calcium changes in neurons Ca2+N and astrocytes Ca2+A, respectively) alongside their vascular interactions in vivo to address this challenge. Using green and red genetically-encoded Ca2+ indicators differentially expressed in astrocytes and neurons, fl-ODM enabled concomitant imaging of large-scale astrocytic and neuronal Ca2+ fluorescence and 3D cerebral blood flow velocity (CBFv) in vascular networks in the mouse cortex. We assessed cocaine's effects in the prefrontal cortex (PFC) and found that the CBFv changes triggered by cocaine were temporally correlated with astrocytic Ca2+A activity. Chemogenetic inhibition of astrocytes during the baseline state resulted in blood vessel dilation and CBFv increases but did not affect neuronal activity, suggesting modulation of spontaneous blood vessel's vascular tone by astrocytes. Chemogenetic inhibition of astrocytes during a cocaine challenge prevented its vasoconstricting effects alongside the CBFv decreases, but it also attenuated the neuronal Ca2+N increases triggered by cocaine. These results document a role of astrocytes both in regulating vascular tone and consequently blood flow, at baseline and for modulating the vasoconstricting and neuronal activation responses to cocaine in the PFC. Strategies to inhibit astrocytic activity could offer promise for ameliorating vascular and neuronal toxicity from cocaine misuse.

Dataset Information

Modification of oxygen consumption and blood flow in mouse somatosensory cortex by cell-type-specific neuronal activity.

Publications

Modification of oxygen consumption and blood flow in mouse somatosensory cortex by cell-type-specific neuronal activity.

Similar Datasets

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