Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity

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Abstract
Functional magnetic resonance imaging (fMRI) of brain activity relies on the assumption that increases in local blood flow in the brain are directly correlated with the neuronal activity in that brain region. Using simultaneous direct recording and fMRI in monkeys, Yevgeniy Sirotin and Aniruddha Das demonstrate that this is not the whole story; part of the fMRI signal is unrelated to actual brain activity. As well as the brain activity component, there is increased blood flow in less active regions of the brain in anticipation of their employment in the near future. These findings challenge to the current interpretation of functional brain imaging signals, and also point to a novel anticipatory mechanism in the brain. Functional magnetic resonance imaging (fMRI) of brain activity relies on the assumption that increases in local blood flow in the brain are directly correlated with the neuronal activity in that brain region. Using simultaneous direct recording and fMRI in monkeys, this study demonstrates that this is not the whole story; some of the fMRI signal does correspond to actual brain activity, but there is also increased blood flow in less active regions of the brain in anticipation of their employment in the near future. 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.