Neural correlates of single-vessel haemodynamic responses in vivo

Philip John O'Herron, Pratik Y. Chhatbar, Manuel Levy, Zhiming Shen, Adrien E. Schramm, Zhongyang Lu, Prakash Kara

Research output: Contribution to journalArticle

68 Citations (Scopus)

Abstract

Neural activation increases blood flow locally. This vascular signal is used by functional imaging techniques to infer the location and strength of neural activity. 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 controversial. 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 exist), 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.

Original languageEnglish (US)
Pages (from-to)378-382
Number of pages5
JournalNature
Volume534
Issue number7607
DOIs
StatePublished - May 25 2016
Externally publishedYes

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Blood Vessels
Hemodynamics
Cats
Arterioles
Visual Cortex
Dilatation
Arteries
Photons
Glutamic Acid
Microscopy
Calcium
Neurons

ASJC Scopus subject areas

  • General

Cite this

O'Herron, P. J., Chhatbar, P. Y., Levy, M., Shen, Z., Schramm, A. E., Lu, Z., & Kara, P. (2016). Neural correlates of single-vessel haemodynamic responses in vivo. Nature, 534(7607), 378-382. https://doi.org/10.1038/nature17965

Neural correlates of single-vessel haemodynamic responses in vivo. / O'Herron, Philip John; Chhatbar, Pratik Y.; Levy, Manuel; Shen, Zhiming; Schramm, Adrien E.; Lu, Zhongyang; Kara, Prakash.

In: Nature, Vol. 534, No. 7607, 25.05.2016, p. 378-382.

Research output: Contribution to journalArticle

O'Herron, PJ, Chhatbar, PY, Levy, M, Shen, Z, Schramm, AE, Lu, Z & Kara, P 2016, 'Neural correlates of single-vessel haemodynamic responses in vivo', Nature, vol. 534, no. 7607, pp. 378-382. https://doi.org/10.1038/nature17965
O'Herron PJ, Chhatbar PY, Levy M, Shen Z, Schramm AE, Lu Z et al. Neural correlates of single-vessel haemodynamic responses in vivo. Nature. 2016 May 25;534(7607):378-382. https://doi.org/10.1038/nature17965
O'Herron, Philip John ; Chhatbar, Pratik Y. ; Levy, Manuel ; Shen, Zhiming ; Schramm, Adrien E. ; Lu, Zhongyang ; Kara, Prakash. / Neural correlates of single-vessel haemodynamic responses in vivo. In: Nature. 2016 ; Vol. 534, No. 7607. pp. 378-382.
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