Anticipatory Hæmodynamic Signals in Sensory Cortex

Hæmodynamic signals underlying functional brain imaging (e.g. fMRI) are assumed to reflect metabolic demand generated by local neuronal activity, with equal increases in hæmodynamic signal implying equal increases in the underlying neuronal activity1-6. Few studies have compared neuronal and hæmodynamic signals in alert animals7,8 to test for this assumed correspondence. Here we present evidence bringing 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 hæmodynamic 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 independent of visual input or of standard neural predictors of hæmodynamics. This latter component shows predictive timing, with increases of cerebral blood volume in anticipation of trial onsets even in darkness. This trial-locked hæmodynamic 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 2 animals) challenge the current understanding of the link between brain hæmodynamics 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.