Haemodynamic signals underlying functional brain imaging (for example, functional magnetic resonance imaging (fMRI)) are assumed to reflect metabolic demand generated by local neuronal activity, with equal increases in haemodynamic signal implying equal increases in the underlying neuronal activity1,2,3,4,5,6. Few studies have compared neuronal and haemodynamic signals in alert animals7,8 to test for this assumed correspondence. Here we present evidence that brings this assumption into question. Using a dual-wavelength optical imaging technique9 that independently measures cerebral blood volume and oxygenation, continuously, in alert behaving monkeys, we find two distinct components to the haemodynamic signal in the alert animals’ primary visual cortex (V1). One component is reliably predictable from neuronal responses generated by visual input. The other component—of almost comparable strength—is a hitherto unknown signal that entrains to task structure independently of visual input or of standard neural predictors of haemodynamics. This latter component shows predictive timing, with increases of cerebral blood volume in anticipation of trial onsets even in darkness. This trial-locked haemodynamic signal could be due to an accompanying V1 arterial pumping mechanism, closely matched in time, with peaks of arterial dilation entrained to predicted trial onsets. These findings (tested in two animals) challenge the current understanding of the link between brain haemodynamics and local neuronal activity. They also suggest the existence of a novel preparatory mechanism in the brain that brings additional arterial blood to cortex in anticipation of expected tasks.
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We thank: K. Korinek for designing and fabricating much of the dual-wavelength optical imaging hardware; P. P. Mitra for the suggestion of making continuous recordings and the use of the Chronux analysis software; E. M. C. Hillman for insights into brain haemodynamic mechanisms; C. Ma, G. Cantone, J. Ordinario, E. Glushenkova, W. Zhang, and M. Bucklin for help with recordings; E. Seidemann and R. Siegel for technical help during our initial setup; C. D. Gilbert and members of the Mahoney Center and the Center for Theoretical Neuroscience at Columbia University for comments on the manuscript. The work was supported by the Keck foundation, grants from the National Institutes of Health, the Klingenstein Foundation, the Gatsby Initiative in Brain Circuitry and the Dana Foundation to A.D. and a National Research Service Award to Y.B.S.
Author Contributions The two co-authors collaborated on almost every aspect of this work.
Supplementary Movie 1 shows high magnification optical images of the trial-linked vascular signal in V1, over the course of one 18.7-sec trial. Left panel: 605 nm. Right panel: 530 nm. Coloured traces show time course of mean signal at each wavelength, with moving cursor indicating phase of currently displayed images. Inset square in upper left shows fixation phase (white: fixate; black: intertrial interval. Time after trial onset, in sec.).