Differential pial and penetrating arterial responses examined by optogenetic activation of astrocytes and neurons

Author:

Hatakeyama Nao1,Unekawa Miyuki2,Murata Juri1,Tomita Yutaka23,Suzuki Norihiro24,Nakahara Jin2,Takuwa Hiroyuki5,Kanno Iwao5ORCID,Matsui Ko6,Tanaka Kenji F7,Masamoto Kazuto158

Affiliation:

1. Graduate School of Informatics and Engineering, University of Electro-Communications, Tokyo, Japan

2. Department of Neurology, Keio University School of Medicine, Tokyo, Japan

3. Tomita Hospital, Aichi, Japan

4. Shonan Keiiku Hospital, Kanagawa, Japan

5. Department of Functional Brain Imaging Research, National Institute of Radiological Sciences, Chiba, Japan

6. Super-Network Brain Physiology, Graduate School of Life Sciences, Tohoku University, Miyagi, Japan

7. Department of Neuropsychiatry, Keio University School of Medicine, Tokyo, Japan

8. Center for Neuroscience and Biomedical Engineering, University of Electro-Communications, Tokyo, Japan

Abstract

A variety of brain cells participates in neurovascular coupling by transmitting and modulating vasoactive signals. The present study aimed to probe cell type-dependent cerebrovascular (i.e., pial and penetrating arterial) responses with optogenetics in the cortex of anesthetized mice. Two lines of the transgenic mice expressing a step function type of light-gated cation channel (channelrhodopsine-2; ChR2) in either cortical neurons (muscarinic acetylcholine receptors) or astrocytes (Mlc1-positive) were used in the experiments. Photo-activation of ChR2-expressing astrocytes resulted in a widespread increase in cerebral blood flow (CBF), extending to the nonstimulated periphery. In contrast, photo-activation of ChR2-expressing neurons led to a relatively localized increase in CBF. The differences in the spatial extent of the CBF responses are potentially explained by differences in the involvement of the vascular compartments. In vivo imaging of the cerebrovascular responses revealed that ChR2-expressing astrocyte activation led to the dilation of both pial and penetrating arteries, whereas ChR2-expressing neuron activation predominantly caused dilation of the penetrating arterioles. Pharmacological studies showed that cell type-specific signaling mechanisms participate in the optogenetically induced cerebrovascular responses. In conclusion, pial and penetrating arterial vasodilation were differentially evoked by ChR2-expressing astrocytes and neurons.

Publisher

SAGE Publications

Subject

Cardiology and Cardiovascular Medicine,Neurology (clinical),Neurology

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