Towards a Neuroscientific Understanding of Voluntary Movements

Famed 20^th century philosopher Ludwig Wittgenstein once asked, “What is leftover if I subtract the fact that my arm goes up from the fact that I raise my arm?” The simple answer is volition—the idea that one chooses to voluntarily raise one’s arm as opposed to it being moved by some external force. Yet, the nature of volition, or so-called “free will,” is something that philosophers and scientists have debated for centuries. Now, neuroscientists are picking up the thread, trying to identify new techniques and methods to address the neural mechanisms that underlie voluntary action as opposed to habits and reflexive movement. Those newer findings were highlighted at Neuroscience 2017, the 47^th annual meeting of the Society for Neuroscience (SfN), in a special session chaired by neurosurgeon Itzhak Fried, called  “Neural Mechanisms of Voluntary Action Control:  From Habits to Intentionality in Animals and Humans.”

The Legacy of Benjamin Libet

How does one operationally define volition? It depends on whom you ask. Fried, introducing the SfN session, says that voluntary action is an “ambiguous entity,” at best.

“Volition, intention, will, free will…This is something for which fields of escalating semantics have been invented,” he joked. But scientists and philosophers cannot even agree on a single term—or even if these different concepts represent the same cognitive action. The tools to study in the brain how these things might be represented, however they were defined, also were lacking.

Nearly 40 years ago, neurologist Benjamin Libet was one of the first to try to test the notion of free will empirically, using electroencephalogram (EEG) measurements. Building on work by Kornhuber & Deecke that described how the motor cortex shows a so-called readiness potential—an increase in brain activity before one makes a movement—Libet hoped to see if he might correlate neural activity with a person’s intention to move. He had study participants track a dot moving around an oscilloscope. The participant was asked to note the position of the moving dot when they became aware of a desire to move their finger. When he looked at the EEG read-outs, he discovered that participants showed heightened activity in motor cortex when they reported that intention.

While Libet’s experiments were remarkable for their time, it’s difficult to say for certain if Libet was actually measuring intention, said Patrick Haggard, a neuroscientist at the University College London during the session.

“To study volition in a scientific manner rather than a metaphysical one, we need appropriate methods for manipulating and measuring the process,” he argued. “If you consider the concept of volition, you have an action for which there is no input. There is no external trigger to make that movement happen. One is choosing to do it without impetus. In neuroscience, we test these kinds of ideas generally by varying our inputs. But how can you manipulate an input that can’t be there? Without that, it is difficult to determine whether a readiness potential actually represents volition itself or simply some kind of preparation for the action that is going to happen.”

Choosing Not to Wait

To get around that difficulty, Haggard devised a different experimental paradigm while measuring brain activity using EEG. Study participants were asked to look at a fixation point in the middle of a circle of dots. After some time, those dots would start to move to the left or right. Participants had to hit a key when they saw the dots start to move to receive a reward.

“The delay here is extremely variable—and it can be extremely long. So we also give participants the option of making a skip response. You can decide not to wait during this very long, very boring time and get a small reward. Or you can wait it out to receive the larger one,” Haggard explained. “Making the skip ticks all the important boxes for what makes up a true voluntary action. It is not triggered by a stimulus. It’s entirely up to you when you skip, or even if you want to skip—it’s a truly internally generated response. And it’s a reasoned response, as well. You are skipping for a reason, to save time.”

When comparing recordings from the supplementary motor cortex during skips versus other trials, Haggard and colleagues discovered a convergence of brain activity into a consistent pattern—which, Haggard argues, suggests there is some kind of volitional cognitive process going on when one makes the decision to skip.

“Just the possibility of making a voluntary action doesn’t cause any change in this convergence of EEG activity,” he said. “It’s the actual event of getting ready to do it.”

To further investigate this phenomenon, Haggard and colleagues repeated the same experiment—except this time, participants had a limited number of skips to use.

“Free will here was rationed. It was valuable commodity,” he says. “It’s something special so you have to really consider and decide, ‘Do I really want to use my skip here?’”

When they analyzed the EEG data for this study, the researchers found that the readiness pattern was slightly stronger than the previous experiment. They also found that the differences in EEG variation among participants dropped prior to the limited skips.

“The impact here is that the skipping is less habitual. You have to think about it more because you don’t have as many chances to skip. It’s more difficult to make the decision,” he explained. “And this seems to increase the drop in neural variability when you achieve this activity convergence.”

Stimulating Volition

Biyu He, a neuroscientist at NYU Langone Health, presented her work using transcranial direct current stimulation (tDCS) to look at voluntary actions in the special SfN session. She argued that several neuropsychiatric conditions, like alien hand syndrome, where a hand functions involuntarily, demonstrate that movement and intention can be dissociated both anatomically and clinically.

“Folk psychology suggests that conscious thought causes actions: I think therefore I do,” she said. “But when you stimulate the premotor cortex you can generate movement without a person’s awareness that they have moved. And you also have different clinical conditions where movement and intention are clearly dissociated.”

He and colleagues recruited 12 participants; half received tDCS stimulation in brain regions implicated in movement intention, including primary motor cortex and angular gyrus, while the others received a sham stimulation. The study participants were then asked to perform the Libet task while an EEG took recordings from those same areas. The researchers then fed those readings into a computational model to look for trends. They discovered that stimulation in the angular gyrus and primary motor cortex resulted in an enhanced readiness potential—starting one to three seconds before movement onset in comparison to those who received the sham stimulation. This, she argued, showed an enhanced sense of volition.

“This work leads us to a hypothesis that disorders with psychogenic movements, like alien hand syndrome, make abnormally low activity in the angular gyrus, which results in weakened movement intention and delays a person’s sense of volition,” she said. “And this work with non-invasive brain stimulation may help us restore a sense of volition in these patients and help mediate the clinical symptoms.”

Moving Forward

Fried said now is the time to start talking more about the neural correlates of voluntary action—with improved experimental paradigms and more advanced technologies, he thinks there is more opportunity to help tease apart the processes that determine voluntary versus habitual movement. Haggard agrees.

“We finally have good methods to study these phenomena properly,” he said. “I’m quite optimistic. I think we can get to the important knowledge we need regarding the brain mechanisms that make an action voluntary. And there is an imperative to do that. It is very relevant to psychiatry and mental health. But it is also relevant to everyday, normal health considering that volition is, after all, the very basis of our society.”