Letter | Published:

Neural correlates of single-vessel haemodynamic responses in vivo

Nature volume 534, pages 378382 (16 June 2016) | Download Citation

Abstract

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 haemodynamic signals is controversial3,4,5,6,7,8,9. Previous studies recorded local field potentials as a measure of synaptic activity together with spiking activity and low-resolution haemodynamic 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 similarly to those for 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. Neighbouring 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 haemodynamic signals were partly decoupled. Together, these results indicate that intrinsic cortical properties, such as propagation of vascular dilation between neighbouring columns, need to be accounted for when decoding haemodynamic signals.

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Acknowledgements

We thank A. Shih for comments on the manuscript. This work was supported by grants from the National Institutes of Health (NS088827), National Science Foundation (1539034), and Whitehall and Dana Foundations to P.K.

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Affiliations

  1. Department of Neuroscience, Medical University of South Carolina, Charleston, South Carolina 29425, USA

    • Philip O’Herron
    • , Pratik Y. Chhatbar
    • , Manuel Levy
    • , Zhiming Shen
    • , Adrien E. Schramm
    • , Zhongyang Lu
    •  & Prakash Kara

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Contributions

P.K. conceived and supervised the project. All authors collected data. P.O’H. and P.Y.C. analysed data. P.O’H., M.L. and P.K. wrote the paper. All authors commented on and approved the final manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Prakash Kara.

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https://doi.org/10.1038/nature17965

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