Vascular Compartmentalization of Functional Hyperemia from the Synapse to the Pia
Functional hyperemia, a regional increase of blood flow triggered by local neural activation, is used to map brain activity in health and disease. However, the spatial-temporal dynamics of functional hyperemia remain unclear. Two-photon imaging of the entire vascular arbor in NG2-creERT2;GCaMP6f mic...
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| Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2018-07, Vol.99 (2), p.362-375.e4 |
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| description | Functional hyperemia, a regional increase of blood flow triggered by local neural activation, is used to map brain activity in health and disease. However, the spatial-temporal dynamics of functional hyperemia remain unclear. Two-photon imaging of the entire vascular arbor in NG2-creERT2;GCaMP6f mice shows that local synaptic activation, measured via oligodendrocyte precursor cell (OPC) Ca2+ signaling, generates a synchronous Ca2+ drop in pericytes and smooth muscle cells (SMCs) enwrapping all upstream vessels feeding the activated synapses. Surprisingly, the onset timing, direction, and amplitude of vessel diameter and blood velocity changes vary dramatically from juxta-synaptic capillaries back to the pial arteriole. These results establish a precise spatial-temporal sequence of vascular changes triggered by neural activity and essential for the interpretation of blood-flow-based imaging techniques such as BOLD-fMRI.
•Odor triggers rapid Ca2+ elevations in OPC process that are input specific•All pericyte subtypes and SMCs respond to downstream synaptic activation•Synchronous mural cell activation is associated with heterogeneous local hemodynamics•The arteriole and first-order capillary dilate first and form the primary functional unit
Rungta et al. perform in vivo two-photon calcium imaging of neuron, oligodendrocyte precursor cell, pericyte, and smooth muscle cell responses to olfactory sensory stimulation in combination with vessel diameter and red blood cell velocity measurements along the entire vascular arbor. |
| doi_str_mv | 10.1016/j.neuron.2018.06.012 |
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•Odor triggers rapid Ca2+ elevations in OPC process that are input specific•All pericyte subtypes and SMCs respond to downstream synaptic activation•Synchronous mural cell activation is associated with heterogeneous local hemodynamics•The arteriole and first-order capillary dilate first and form the primary functional unit
Rungta et al. perform in vivo two-photon calcium imaging of neuron, oligodendrocyte precursor cell, pericyte, and smooth muscle cell responses to olfactory sensory stimulation in combination with vessel diameter and red blood cell velocity measurements along the entire vascular arbor.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2018.06.012</identifier><identifier>PMID: 29937277</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>anesthetized ; Animals ; astrocyte ; awake ; Blood flow ; blood-brain barrier ; Brain - blood supply ; Brain - physiology ; Brain Chemistry - physiology ; Brain mapping ; calcium ; Calcium signalling ; Capillaries ; CBF ; endothelium ; functional imaging ; Functional magnetic resonance imaging ; gap junction ; glia ; glutamate ; Hyperemia ; Hyperemia - diagnosis ; Hyperemia - physiopathology ; hyperpolarization ; in vivo ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Microscopy, Confocal - methods ; microvascular ; Muscle, Smooth, Vascular - chemistry ; Muscle, Smooth, Vascular - physiology ; Neuroimaging ; neuron ; neurovascular coupling ; neurovascular unit ; odor ; Odors ; Pericytes ; Pericytes - chemistry ; Pericytes - physiology ; Pia Mater - blood supply ; Pia Mater - chemistry ; Pia Mater - physiology ; Smooth muscle ; Synapses ; Synapses - chemistry ; Synapses - physiology ; Velocity</subject><ispartof>Neuron (Cambridge, Mass.), 2018-07, Vol.99 (2), p.362-375.e4</ispartof><rights>2018 The Authors</rights><rights>Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.</rights><rights>2018. The Authors</rights><rights>2018 The Authors 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c557t-596d27d8dafc4d81bb20e4f49b35b56316bec1d25d27626caa9dc5ce9826c1c93</citedby><cites>FETCH-LOGICAL-c557t-596d27d8dafc4d81bb20e4f49b35b56316bec1d25d27626caa9dc5ce9826c1c93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S089662731830480X$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29937277$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Rungta, Ravi L.</creatorcontrib><creatorcontrib>Chaigneau, Emmanuelle</creatorcontrib><creatorcontrib>Osmanski, Bruno-Félix</creatorcontrib><creatorcontrib>Charpak, Serge</creatorcontrib><title>Vascular Compartmentalization of Functional Hyperemia from the Synapse to the Pia</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Functional hyperemia, a regional increase of blood flow triggered by local neural activation, is used to map brain activity in health and disease. However, the spatial-temporal dynamics of functional hyperemia remain unclear. Two-photon imaging of the entire vascular arbor in NG2-creERT2;GCaMP6f mice shows that local synaptic activation, measured via oligodendrocyte precursor cell (OPC) Ca2+ signaling, generates a synchronous Ca2+ drop in pericytes and smooth muscle cells (SMCs) enwrapping all upstream vessels feeding the activated synapses. Surprisingly, the onset timing, direction, and amplitude of vessel diameter and blood velocity changes vary dramatically from juxta-synaptic capillaries back to the pial arteriole. These results establish a precise spatial-temporal sequence of vascular changes triggered by neural activity and essential for the interpretation of blood-flow-based imaging techniques such as BOLD-fMRI.
•Odor triggers rapid Ca2+ elevations in OPC process that are input specific•All pericyte subtypes and SMCs respond to downstream synaptic activation•Synchronous mural cell activation is associated with heterogeneous local hemodynamics•The arteriole and first-order capillary dilate first and form the primary functional unit
Rungta et al. perform in vivo two-photon calcium imaging of neuron, oligodendrocyte precursor cell, pericyte, and smooth muscle cell responses to olfactory sensory stimulation in combination with vessel diameter and red blood cell velocity measurements along the entire vascular arbor.</description><subject>anesthetized</subject><subject>Animals</subject><subject>astrocyte</subject><subject>awake</subject><subject>Blood flow</subject><subject>blood-brain barrier</subject><subject>Brain - blood supply</subject><subject>Brain - physiology</subject><subject>Brain Chemistry - physiology</subject><subject>Brain mapping</subject><subject>calcium</subject><subject>Calcium signalling</subject><subject>Capillaries</subject><subject>CBF</subject><subject>endothelium</subject><subject>functional imaging</subject><subject>Functional magnetic resonance imaging</subject><subject>gap junction</subject><subject>glia</subject><subject>glutamate</subject><subject>Hyperemia</subject><subject>Hyperemia - diagnosis</subject><subject>Hyperemia - physiopathology</subject><subject>hyperpolarization</subject><subject>in vivo</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Microscopy, Confocal - methods</subject><subject>microvascular</subject><subject>Muscle, Smooth, Vascular - chemistry</subject><subject>Muscle, Smooth, Vascular - physiology</subject><subject>Neuroimaging</subject><subject>neuron</subject><subject>neurovascular coupling</subject><subject>neurovascular unit</subject><subject>odor</subject><subject>Odors</subject><subject>Pericytes</subject><subject>Pericytes - chemistry</subject><subject>Pericytes - physiology</subject><subject>Pia Mater - blood supply</subject><subject>Pia Mater - chemistry</subject><subject>Pia Mater - physiology</subject><subject>Smooth muscle</subject><subject>Synapses</subject><subject>Synapses - chemistry</subject><subject>Synapses - physiology</subject><subject>Velocity</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU1v1DAQhi0EotvCP0AoEhcuCbbjj_iChFYtRaoEiI-r5dgT6lViBzuptPx6vN1SPg6cZkZ-5vXMvAg9I7ghmIhXuybAmmJoKCZdg0WDCX2ANgQrWTOi1EO0wZ0StaCyPUGnOe8wJowr8hidUKVaSaXcoI9fTbbraFK1jdNs0jJBWMzof5jFx1DFobpYgz3kZqwu9zMkmLyphhSnarmG6tM-mDlDtcTb8oM3T9CjwYwZnt7FM_Tl4vzz9rK-ev_23fbNVW05l0vNlXBUus6ZwTLXkb6nGNjAVN_ynouWiB4scZQXSlBhjVHOcguqKwWxqj1Dr4-689pP4GyZO5lRz8lPJu11NF7__RL8tf4Wb7TAQgnJisDLO4EUv6-QFz35bGEcTYC4Zk0xV5i1gsmCvvgH3cU1lZMcKCmI5J1sC8WOlE0x5wTD_TAE64NneqePnumDZxoLXTwrbc__XOS-6ZdJvzeFcs4bD0ln6yFYcD6BXbSL_v8__ARYHavL</recordid><startdate>20180725</startdate><enddate>20180725</enddate><creator>Rungta, Ravi L.</creator><creator>Chaigneau, Emmanuelle</creator><creator>Osmanski, Bruno-Félix</creator><creator>Charpak, Serge</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><general>Cell Press</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20180725</creationdate><title>Vascular Compartmentalization of Functional Hyperemia from the Synapse to the Pia</title><author>Rungta, Ravi L. ; Chaigneau, Emmanuelle ; Osmanski, Bruno-Félix ; Charpak, Serge</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c557t-596d27d8dafc4d81bb20e4f49b35b56316bec1d25d27626caa9dc5ce9826c1c93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>anesthetized</topic><topic>Animals</topic><topic>astrocyte</topic><topic>awake</topic><topic>Blood flow</topic><topic>blood-brain barrier</topic><topic>Brain - blood supply</topic><topic>Brain - physiology</topic><topic>Brain Chemistry - physiology</topic><topic>Brain mapping</topic><topic>calcium</topic><topic>Calcium signalling</topic><topic>Capillaries</topic><topic>CBF</topic><topic>endothelium</topic><topic>functional imaging</topic><topic>Functional magnetic resonance imaging</topic><topic>gap junction</topic><topic>glia</topic><topic>glutamate</topic><topic>Hyperemia</topic><topic>Hyperemia - diagnosis</topic><topic>Hyperemia - physiopathology</topic><topic>hyperpolarization</topic><topic>in vivo</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Transgenic</topic><topic>Microscopy, Confocal - methods</topic><topic>microvascular</topic><topic>Muscle, Smooth, Vascular - chemistry</topic><topic>Muscle, Smooth, Vascular - physiology</topic><topic>Neuroimaging</topic><topic>neuron</topic><topic>neurovascular coupling</topic><topic>neurovascular unit</topic><topic>odor</topic><topic>Odors</topic><topic>Pericytes</topic><topic>Pericytes - chemistry</topic><topic>Pericytes - physiology</topic><topic>Pia Mater - blood supply</topic><topic>Pia Mater - chemistry</topic><topic>Pia Mater - physiology</topic><topic>Smooth muscle</topic><topic>Synapses</topic><topic>Synapses - chemistry</topic><topic>Synapses - physiology</topic><topic>Velocity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rungta, Ravi L.</creatorcontrib><creatorcontrib>Chaigneau, Emmanuelle</creatorcontrib><creatorcontrib>Osmanski, Bruno-Félix</creatorcontrib><creatorcontrib>Charpak, Serge</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Rungta, Ravi L.</au><au>Chaigneau, Emmanuelle</au><au>Osmanski, Bruno-Félix</au><au>Charpak, Serge</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Vascular Compartmentalization of Functional Hyperemia from the Synapse to the Pia</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2018-07-25</date><risdate>2018</risdate><volume>99</volume><issue>2</issue><spage>362</spage><epage>375.e4</epage><pages>362-375.e4</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>Functional hyperemia, a regional increase of blood flow triggered by local neural activation, is used to map brain activity in health and disease. However, the spatial-temporal dynamics of functional hyperemia remain unclear. Two-photon imaging of the entire vascular arbor in NG2-creERT2;GCaMP6f mice shows that local synaptic activation, measured via oligodendrocyte precursor cell (OPC) Ca2+ signaling, generates a synchronous Ca2+ drop in pericytes and smooth muscle cells (SMCs) enwrapping all upstream vessels feeding the activated synapses. Surprisingly, the onset timing, direction, and amplitude of vessel diameter and blood velocity changes vary dramatically from juxta-synaptic capillaries back to the pial arteriole. These results establish a precise spatial-temporal sequence of vascular changes triggered by neural activity and essential for the interpretation of blood-flow-based imaging techniques such as BOLD-fMRI.
•Odor triggers rapid Ca2+ elevations in OPC process that are input specific•All pericyte subtypes and SMCs respond to downstream synaptic activation•Synchronous mural cell activation is associated with heterogeneous local hemodynamics•The arteriole and first-order capillary dilate first and form the primary functional unit
Rungta et al. perform in vivo two-photon calcium imaging of neuron, oligodendrocyte precursor cell, pericyte, and smooth muscle cell responses to olfactory sensory stimulation in combination with vessel diameter and red blood cell velocity measurements along the entire vascular arbor.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>29937277</pmid><doi>10.1016/j.neuron.2018.06.012</doi><oa>free_for_read</oa></addata></record> |
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| subjects | anesthetized Animals astrocyte awake Blood flow blood-brain barrier Brain - blood supply Brain - physiology Brain Chemistry - physiology Brain mapping calcium Calcium signalling Capillaries CBF endothelium functional imaging Functional magnetic resonance imaging gap junction glia glutamate Hyperemia Hyperemia - diagnosis Hyperemia - physiopathology hyperpolarization in vivo Mice Mice, Inbred C57BL Mice, Transgenic Microscopy, Confocal - methods microvascular Muscle, Smooth, Vascular - chemistry Muscle, Smooth, Vascular - physiology Neuroimaging neuron neurovascular coupling neurovascular unit odor Odors Pericytes Pericytes - chemistry Pericytes - physiology Pia Mater - blood supply Pia Mater - chemistry Pia Mater - physiology Smooth muscle Synapses Synapses - chemistry Synapses - physiology Velocity |
| title | Vascular Compartmentalization of Functional Hyperemia from the Synapse to the Pia |
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