Another shock for brain imaging research - the signal isn't always linked to neuronal activity

The brain imaging community is about to experience another shockwave, just days after the online leak of a paper that challenged many of the brain-behaviour correlations reported in respected social neuroscience journals.

Now Yevgeniy Sirotin and Aniruddha Das have reported that blood flow changes in the brain - the signal measured by brain scanners - are not always linked to changes in neuronal activity. Experts have known for some time that the relationship between blood flow and neuronal activity might be rather complicated but this is the first time that such an extreme mismatch has been demonstrated.

Sirotin and Das used electrodes to directly record neuronal activity in the vision part of the brains of two awake monkeys, and at the same time they used a camera system and injected dyes to monitor blood flow to that region. This kind of thing couldn't be done with humans because it is too intrusive and physically harmful.

The monkeys were trained to look at a tiny dot when it was one colour and to relax when it was another colour. The dot alternated colours following a predictable rhythm, so the monkeys could predict when they'd need to concentrate and when they could relax. Sometimes, when the monkeys were required to fixate the dot, it was accompanied by intense visual stimuli, whereas on other trials there was nothing, leaving the monkeys in near darkness.

As you'd expect, when there was intense visual stimulation, the researchers observed increased neuronal activity in the visual area of the monkeys' brains and lots of blood flow to that region. But here's the important bit: they also observed increased blood flow to the visual brain even when there was nothing for the monkeys to look at, except for the minuscule dot, and even though neuronal activity was virtually silent. It's as though extra blood was being channelled to the visual cortex, in anticipation that there might be lots of visual material to look at.

There's a chance that this anticipatory blood flow could just reflect an increase in arousal, since the researchers also noted anticipatory changes to heart rate and pupil size just before an active phase of each trial was due to begin. However, Sirotin and Das were able to rule this out using an auditory task. Heart rate and pupil size changed in anticipation of the active phase of the auditory task, but there was no anticipatory blood flow to the visual parts of the brain.

The interpretation of human brain imaging experiments is founded on the idea that changes in blood flow reflect parallel changes in neuronal activity. This important new study shows that blood flow changes can be anticipatory and completely unconnected to any localised neuronal activity. It's up to future research to find out which brain areas and cognitive mechanisms are controlling this anticipatory blood flow. As the researchers said, their finding points to a "novel anticipatory brain mechanism".

Writing a commentary on this paper in the same journal issue, David Leopold at the National Institute of Mental Health, Bethesda, said the findings were "sure to raise eyebrows among the human fMRI research community."
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Yevgeniy B. Sirotin, Aniruddha Das (2009). Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity. Nature, 457, 475-479.

Image shows blood vessel activation in the brain evoked by visual stimulus. White lightning bolt patterns outline arteries in the contraction phase of the anticipatory response; dark centre is the specific response to the visual stimulus. Credit Sirotin & Das.

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