Brain might not stand in the way of free will

Advocates of free will can rest easy, for now. A 30-year-old classic experiment that is often used to argue against free will might have been misinterpreted.

In the early 1980s, Benjamin Libet, a neuroscientist at the University of California in San Francisco, used electroencephalography (EEG) to record the brain activity of volunteers who had been told to make a spontaneous movement. With the help of a precise timer that the volunteers were asked to read at the moment they became aware of the urge to act, Libet found there was a 200 millisecond delay, on average, between this urge and the movement itself.

But the EEG recordings also revealed a signal that appeared in the brain even earlier, 550 milliseconds, on average, before the action. Called the readiness potential, this has been interpreted as a blow to free will, as it suggests that the brain prepares to act well before we are conscious of the urge to move.

This conclusion assumes that the readiness potential is the signature of the brain planning and preparing to move. "Even people who have been critical of Libet's work, by and large, haven't challenged that assumption," says Aaron Schurger of the National Institute of Health and Medical Research in Saclay, France.

One attempt to do so came in 2009. Judy Trevena and Jeff Miller of the University of Otago in Dunedin, New Zealand, asked volunteers to decide, after hearing a tone, whether or not to tap on a keyboard. The readiness potential was present regardless of their decision, suggesting that it did not represent the brain preparing to move. Exactly what it did mean, though, still wasn't clear.

Crossing a threshold

Now, Schurger and colleagues have an explanation. They began by posing a question: how does the brain decide to make a spontaneous movement? They looked to other decision-making scenarios for clues. Previous studies have shown that when we have to make a decision based on visual input, for example, assemblies of neurons start accumulating visual evidence in favour of the various possible outcomes. A decision is triggered when the evidence favouring one particular outcome becomes strong enough to tip its associated assembly of neurons across a threshold.

Schurger's team hypothesised that something similar happens in the brain during the Libet experiment. Volunteers, however, are specifically asked to ignore any external signals before they make a spontaneous movement, so the signal must be internal.

There are random fluctuations of neural activity in the brain. Schurger's team reasoned that movement is triggered when this neural noise accumulates and crosses a threshold.

To probe the idea, the team first built a computer model of such a neural accumulator. In the model, each time the neural noise crossed a threshold it signified a decision to move. They found that when they ran the model numerous times and looked at the pattern of the neural noise that led up to the decision it looked like a readiness potential.

Next, the team repeated Libet's experiment, but this time if, while waiting to act spontaneously, the volunteers heard a click they had to act immediately. The researchers predicted that the fastest response to the click would be seen in those in whom the accumulation of neural noise had neared the threshold ? something that would show up in their EEG as a readiness potential.

This is exactly what the team found. In those with slower responses to the click, the readiness potential was absent in the EEG recordings.

Spontaneous brain activity

"Libet argued that our brain has already decided to move well before we have a conscious intention to move," says Schurger. "We argue that what looks like a pre-conscious decision process may not in fact reflect a decision at all. It only looks that way because of the nature of spontaneous brain activity."

So what does this say about free will? "If we are correct, then the Libet experiment does not count as evidence against the possibility of conscious will," says Schurger.

Cognitive neuroscientist Anil Seth of the University of Sussex in Brighton, UK, is impressed by the work, but also circumspect about what it says about free will. "It's a more satisfying mechanistic explanation of the readiness potential. But it doesn't bounce conscious free will suddenly back into the picture," he says. "Showing that one aspect of the Libet experiment can be open to interpretation does not mean that all arguments against conscious free will need to be ejected."

According to Seth, when the volunteers in Libet's experiment said they felt an urge to act, that urge is an experience, similar to an experience of smell or taste. The new model is "opening the door towards a richer understanding of the neural basis of the conscious experience of volition", he says.

Journal reference: Proceedings of the National Academy of Sciences, DOI: 10.1073.pnas.1210467109

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