Neural correlates of single vessel hemodynamic responses in vivo

Neural activation increases blood flow locally. This vascular signal is used by functional imaging techniques to infer the location and strength of neural activity1,2. However, the precise spatial scale over which neural and vascular signals are correlated is unknown. Furthermore, the relative role...

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Main Authors:	O'Herron, Philip, Chhatbar, Pratik Y, Levy, Manuel, Shen, Zhiming, Schramm, Adrien E, Lu, Zhongyang, Kara, Prakash
Format:	Online
Language:	English
Published:	2016
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4911280/

id	pubmed-4911280
recordtype	oai_dc
spelling	pubmed-49112802016-11-25 Neural correlates of single vessel hemodynamic responses in vivo O'Herron, Philip Chhatbar, Pratik Y Levy, Manuel Shen, Zhiming Schramm, Adrien E Lu, Zhongyang Kara, Prakash Article Neural activation increases blood flow locally. This vascular signal is used by functional imaging techniques to infer the location and strength of neural activity1,2. However, the precise spatial scale over which neural and vascular signals are correlated is unknown. Furthermore, the relative role of synaptic and spiking activity in driving hemodynamic signals is controversial3-9. Prior studies recorded local field potentials (LFPs) as a measure of synaptic activity together with spiking activity and low-resolution hemodynamic imaging. Here we used two-photon microscopy to measure sensory-evoked responses of individual blood vessels (dilation, blood velocity) while imaging synaptic and spiking activity in the surrounding tissue using fluorescent glutamate and calcium sensors. In cat primary visual cortex, where neurons are clustered by their preference for stimulus orientation, we discovered new maps for excitatory synaptic activity, which were organized similar to spiking activity but were less selective for stimulus orientation and direction. We generated tuning curves for individual vessel responses for the first time and found that parenchymal vessels in cortical layer 2/3 were orientation selective. Neighboring penetrating arterioles had different orientation preferences. Pial surface arteries in cats, as well as surface arteries and penetrating arterioles in rat visual cortex (where orientation maps do not exist10), responded to visual stimuli but had no orientation selectivity. We integrated synaptic or spiking responses around individual parenchymal vessels in cats and established that the vascular and neural responses had the same orientation preference. However, synaptic and spiking responses were more selective than vascular responses—vessels frequently responded robustly to stimuli that evoked little to no neural activity in the surrounding tissue. Thus, local neural and hemodynamic signals were partly decoupled. Together, these results indicate that intrinsic cortical properties, such as propagation of vascular dilation between neighboring columns, need to be accounted for when decoding hemodynamic signals. 2016-05-25 /pmc/articles/PMC4911280/ /pubmed/27281215 http://dx.doi.org/10.1038/nature17965 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	O'Herron, Philip Chhatbar, Pratik Y Levy, Manuel Shen, Zhiming Schramm, Adrien E Lu, Zhongyang Kara, Prakash
spellingShingle	O'Herron, Philip Chhatbar, Pratik Y Levy, Manuel Shen, Zhiming Schramm, Adrien E Lu, Zhongyang Kara, Prakash Neural correlates of single vessel hemodynamic responses in vivo
author_facet	O'Herron, Philip Chhatbar, Pratik Y Levy, Manuel Shen, Zhiming Schramm, Adrien E Lu, Zhongyang Kara, Prakash
author_sort	O'Herron, Philip
title	Neural correlates of single vessel hemodynamic responses in vivo
title_short	Neural correlates of single vessel hemodynamic responses in vivo
title_full	Neural correlates of single vessel hemodynamic responses in vivo
title_fullStr	Neural correlates of single vessel hemodynamic responses in vivo
title_full_unstemmed	Neural correlates of single vessel hemodynamic responses in vivo
title_sort	neural correlates of single vessel hemodynamic responses in vivo
description	Neural activation increases blood flow locally. This vascular signal is used by functional imaging techniques to infer the location and strength of neural activity1,2. However, the precise spatial scale over which neural and vascular signals are correlated is unknown. Furthermore, the relative role of synaptic and spiking activity in driving hemodynamic signals is controversial3-9. Prior studies recorded local field potentials (LFPs) as a measure of synaptic activity together with spiking activity and low-resolution hemodynamic imaging. Here we used two-photon microscopy to measure sensory-evoked responses of individual blood vessels (dilation, blood velocity) while imaging synaptic and spiking activity in the surrounding tissue using fluorescent glutamate and calcium sensors. In cat primary visual cortex, where neurons are clustered by their preference for stimulus orientation, we discovered new maps for excitatory synaptic activity, which were organized similar to spiking activity but were less selective for stimulus orientation and direction. We generated tuning curves for individual vessel responses for the first time and found that parenchymal vessels in cortical layer 2/3 were orientation selective. Neighboring penetrating arterioles had different orientation preferences. Pial surface arteries in cats, as well as surface arteries and penetrating arterioles in rat visual cortex (where orientation maps do not exist10), responded to visual stimuli but had no orientation selectivity. We integrated synaptic or spiking responses around individual parenchymal vessels in cats and established that the vascular and neural responses had the same orientation preference. However, synaptic and spiking responses were more selective than vascular responses—vessels frequently responded robustly to stimuli that evoked little to no neural activity in the surrounding tissue. Thus, local neural and hemodynamic signals were partly decoupled. Together, these results indicate that intrinsic cortical properties, such as propagation of vascular dilation between neighboring columns, need to be accounted for when decoding hemodynamic signals.
publishDate	2016
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4911280/
_version_	1613596046918680576

Neural correlates of single vessel hemodynamic responses in vivo

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