Haven you ever wondered what goes on in a monkey’s mind when it’s making a decision? We haven’t either. But for Stanford University neuroscientists, doing exactly that could help design better prostheses (such as artificial arms) controlled by a user’s brain.

For example, when should the artificial arm move? Instantly, or only after the user is absolutely certain of a decision (as indicated by neural signals) to avoid a premature or “oops” move?

To find out, the researchers, led by electrical engineering Professor Krishna Shenoy, wired up the monkeys with 192 electrodes in each monkey’s dorsal premotor cortex and primary motor cortex — brain areas centrally involved in preparing and producing the movements execute decisions. “When a monkey is instructed about an upcoming movement but not yet allowed to make it, neurons in these areas show changes in firing rate that reflect the properties of the upcoming reach, including direction,” the researchers state in an open-access paper in the journal eLife.

They also designed a new “single trial decoder” algorithm that does a moment-by-moment analysis of brain activity each time a laboratory monkey reaches out during an experiment, revealing the neural signals that occurred during a momentary hesitation or when the monkey changed his mind.

The experiment

The actual experiment* was performed by neuroscientist Matthew Kaufman, now a postdoctoral scholar at Cold Spring Harbor Laboratory, while he was a graduate student in Shenoy’s lab. “We are seeing many cognitive phenomena in the brain for the first time,” said Kaufman. “The most critical result of our work here is that we can track a single decision and see how the monkey arrived there: whether he decided quickly, slowly, or changed his mind halfway through.

In previous experiments on decision-making, researchers have had monkeys perform many trials and average the readings they obtain to get summary statistics. But these older approaches do not allow researchers to identify unique or idiosyncratic events during any individual decision.

“We can now track single decisions with unprecedented precision,” Kaufman said. “We saw that the brain activity for a typical free choice looked just like it did for a forced choice. But a few of the free choices were different. Occasionally, he was indecisive for a moment before he made any plan at all. About one time in eight, he made a plan quickly but spontaneously changed his mind a moment later.”

This deeper understanding of decision-making promises to help researchers fine-tune the control algorithms of neural prostheses to enable people with paralysis to drive a brain-controlled prosthetic arm or guide a neurally-activated cursor on a computer screen.

Implications for the classic “free will” debate

Kaufman said the team’s findings also bear on a longstanding philosophical debate about human consciousness.

In the early 1980s, University of California, San Francisco neuroscientist Benjamin Libet conducted an experiment to assess the nature of free will. Subjects hooked up to an electroencephalogram (EEG) were asked to push a button whenever they liked. They were also asked to note the precise time that they first became aware of the wish or urge to move.

Libet’s experiments showed that distinctive brain activity began, on average, several seconds before subjects became aware that they planned to move. Libet concluded that the desire to move arose unconsciously, and “free will” could only come in the form of a conscious veto: what he called “free won’t.”

Kaufman said that the brain activity Libet saw does not imply a demise of free will. Instead, his results show that you can plan to make a particular movement, but sometimes change your mind a second later. The moment of commitment to your choice might therefore happen late, just as Libet’s subjects reported. “Being able to see how each choice unfolds on a millisecond timescale may help make it possible to better study these kinds of slippery issues,” Kaufman said.

The work was supported in part by a Director’s Pioneer Award from the National Institutes of Health and by a REPAIR grant from the Defense Advanced Research Projects Agency.

* The experiments involved monkeys that were trained to reach for either of two targets on a computer screen. It was often possible to reach either target, inviting a free choice. Sometimes, one target was blocked, resulting in a forced choice. Other times, the researchers would switch between these configurations while the monkey was deciding, encouraging a change of mind.

The research focused on the time the monkey spent deliberating, before the actual movement began. The monkeys were trained to sit motionless while two jittering targets were positioned on either side of a computer screen.

Colored barriers on the screen created a simple maze. When the targets stopped jittering the monkeys were trained to move to one or the other target by sweeping his fingertip through the maze until he touched one of the targets.

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Abstract of Vacillation, indecision and hesitation in moment-by-moment decoding of monkey motor cortex

When choosing actions, we can act decisively, vacillate, or suffer momentary indecision. Studying how individual decisions unfold requires moment-by-moment readouts of brain state. Here we provide such a view from dorsal premotor and primary motor cortex. Two monkeys performed a novel decision task while we recorded from many neurons simultaneously. We found that a decoder trained using ‘forced choices’ (one target viable) was highly reliable when applied to ‘free choices’. However, during free choices internal events formed three categories. Typically, neural activity was consistent with rapid, unwavering choices. Sometimes, though, we observed presumed ‘changes of mind’: the neural state initially reflected one choice before changing to reflect the final choice. Finally, we observed momentary ‘indecision’: delay forming any clear motor plan. Further, moments of neural indecision accompanied moments of behavioral indecision. Together, these results reveal the rich and diverse set of internal events long suspected to occur during free choice.