Investigators for the first time have used electrode recordings of the firing patterns of small clusters of neurons to predict voluntary movement in people more than 1 second before they are even aware of their decision or urge to act.
The experiment, conducted by Dr. Itzhak Fried of the University of California, Los Angeles, and his associates, detected sets of neurons in the supplementary and presupplementary motor areas and the anterior cingulate cortex (ACC) with firing rates that would progressively increase or decrease before the participants had even reported the urge to push a button on a laptop.
The investigators then constructed algorithms that could successfully predict the impending decision to move at a rate of 70% or greater, depending on the location and size of the set of neurons chosen (Neuron 2011;69:548-62).
Dr. Fried and his colleagues recruited 12 patients with drug-refractory epilepsy who had chronic depth electrodes implanted to determine their seizure focus for possible surgical resection. While the patients sat in bed, they watched an analog clock on a laptop computer and were instructed to push a button after at least one rotation of the clock's hand whenever “they felt the urge to do so.” Each time that the individuals pushed the button, called time P, the researchers asked them to indicate where the clock handle had been when they first felt the urge to move, called time W.
The participants reported a mean W time of 193 ms prior to P, but this varied from trial to trial. In the trials, the greatest proportion of neurons that changed their activity before W was located in parts of the medial frontal lobe of the brain: the supplementary motor area (SMA), the pre-SMA, and the dorsal and rostral regions of the ACC. In some of these areas, the researchers observed rises in neuronal firing rates beginning several hundreds to several thousands of milliseconds prior to W, whereas progressive declines in firing rates were recorded in a similar time span prior to W. The number of neurons that changed their firing rate also increased as W approached.
The study data did not indicate that the subjects were cued to respond by the completion of the clock hand's first rotation. To sort out concerns related to potentially inaccurate reporting of W and the subjective nature of its determination, the investigators' manipulated the timing of W either forward or backward in time by fixed amounts or by adjusting its timing by a random amount. These analyses indicated that small temporal shifts in W on the order of 200 ms or less are still compatible with the changes in firing rates seen in recorded neurons and matched what was observed within each participant's trials.
With an algorithm that considered the responses of electrodes to be independent of each other across all participants, Dr. Fried and his associates found that they could predict W on a trial-by-trial basis across all participants. The algorithm could detect changes in the neural activity of 512 neurons in frontal lobe regions 500 ms before W in nearly 90% of the trials. The changes in activity could be detected in more than 70% of trials at 1,000 ms before W.
When the algorithm was constructed on the basis of firing patterns from 256 neurons in the SMA, it detected the neurons' change in activity at 500 ms before W in more than 80% of the trials. In comparison, the change in activity of 256 neurons in the ACC at 500 ms before W could be detected in only 70% of trials.
The research was supported by federal grants, the Klingenstein Fund, the Whitehall Foundation, and a Human Frontiers Science Programs Organization fellowship.
Minding Your Brain's Free Will
Neurologists, physiologists, and philosophers were tossed a hot potato in 1983 with Benjamin Libet, Ph.D., and his colleagues' publication of the first attempt to measure the time of the perception of intent to make a “voluntary” movement (Brain 1983;106:623-42). Called W, it happened about 250 ms prior to the movement itself. They compared this time to the onset of the Bereitschaftspotential or Readiness potential (RP), an EEG potential that had been previously described by Dr. Hans Kornhuber and Dr. Lüder Deecke (Pflugers Arch. Gesamte Physiol. Menschen Tiere 1965;284:1-17). The RP starts about a second prior to movement. This was a shock. It appeared that the brain was preparing to make a “voluntary” movement before the person was aware of it! The experiment has been repeated many times, so there is no disputing the data; the controversy is the interpretation.