Neural correlates of single-vessel haemodynamic responses in vivo

• Published in: Nature (London) Vol. 534; no. 7607; pp. 378 - 382
• Main Authors: O’Herron, Philip, Chhatbar, Pratik Y., Levy, Manuel, Shen, Zhiming, Schramm, Adrien E., Lu, Zhongyang, Kara, Prakash
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 16-06-2016; Nature Publishing Group
• Subjects: 14; 14/34; 14/69; 631/378/2607; 631/378/3917; Action Potentials; Animals; Arterioles - physiology; Blood; Blood Vessels - physiology; Calcium - analysis; Calcium - metabolism; Calcium Signaling; Cats; Evoked potentials (Electrophysiology); Evoked Potentials, Somatosensory; Glutamic Acid - metabolism; Hemodynamics; Humanities and Social Sciences; letter; Male; Microscopy, Fluorescence, Multiphoton; Models, Neurological; multidisciplinary; Neural circuitry; Neural transmission; Neurons; Neurons - physiology; Observations; Orientation; Photic Stimulation; Physiological aspects; Rats; Science; Signal transduction; Synapses - metabolism; Variance analysis; Vasodilation; Veins & arteries; Visual Cortex - blood supply; Visual Cortex - cytology; Visual Cortex - physiology
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature17965

Functional imaging techniques use changes in blood flow to infer neural activity, but how strongly the two are correlated is a subject of debate; here, vascular and neural responses to a range of visual stimuli are imaged in cat and rat primary visual cortex, revealing that vascular signals are partially decoupled from local neural signals.
Haemodynamic signals and neural function
Functional imaging techniques exploit changes in blood flow to infer neural activity, but how strongly the two are correlated is a subject of debate. Prakash Kara and colleagues imaged vascular and neural responses to a range of visual stimuli in cat and rat primary visual cortex. Responses of parenchymal vessels in cat visual cortex displayed similar orientation preference as both spiking activity and synaptic activity in the surrounding tissue, but showed less orientation selectivity. Accordingly, parenchymal vessels in cat visual cortex could respond to sensory stimuli that evoked little or no neural activity in the surrounding tissue. Surface arteries in cat and rat visual cortex or parenchymal arteries in rat visual cortex (which does not contain orientation maps) did not show any orientation selectivity. This study indicates that vascular signals are partially decoupled from local neural signals.
Neural activation increases blood flow locally. This vascular signal is used by functional imaging techniques to infer the location and strength of neural activity
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. 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
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. 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
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), 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.