Chun Siong Soon1,2, Marcel Brass1,3, Hans-Jochen Heinze4 & John-Dylan Haynes1,2
There has been a long controversy as to whether subjectively ‘free’ decisions are determined by brain activity ahead of time. We found that the outcome of a decision can be encoded in brain activity of prefrontal and parietal cortex up to 10 s before it enters awareness. This delay presumably reflects the operation of a network of high-level control areas that begin to prepare an upcoming decision long before it enters awareness.
The impression that we are able to freely choose between different possible courses of action is fundamental to our mental life. However, it has been suggested that this subjective experience of freedom is no more than an illusion and that our actions are initiated by unconscious mental processes long before we become aware of our intention to act; 1–3. In a previous experiment, 1, electrical brain activity was recorded while subjects were asked to press a button as soon as they felt the urge to do so. Notably, their conscious decision to press the button was preceded by a few hundred milliseconds by a negative brain potential, the so-called ‘readiness potential’ that originates from the supplementary motor area (SMA), a brain region involved in motor preparation.
Because brain activity in the SMA consistently preceded the conscious decision, it has been argued that the brain had already unconsciously made a decision to move even before the subject became aware of it. However, these intriguing experiments have left a number of controversial questions open; 4–6.
First, the readiness potential is generated by the SMA, and hence only provides information about late stages of motor planning. Thus, it is unclear whether the SMA is indeed the cortical site where the decision for a movement originates 7 or whether high-level planning stages might be involved in unconsciously preparing the decision 8, as was seen in studies on conscious action planning; 9–12.
Second, the time delay between the onset of the readiness potential and the decision is only a few hundred milliseconds; 1. It has been repeatedly argued that potential inaccuracies in the behavioral measurement of the decision time at such short delays could lead one to misjudge the relative timing of brain activity and intention; 3–6.
Third, does any leading brain activity indeed selectively predict the specific outcome of a choice ahead of time? To rule out the idea that any leading activity merely reflects unspecific preparatory activation, 13, it is necessary to study free decisions between more than one behavioral option; 11,14.
Here we directly investigated which regions of the brain predetermine conscious intentions and the time at which they start shaping a motor decision. Subjects who gave informed written consent carried out a freely paced motor-decision task while their brain activity was measured using functional magnetic resonance imaging (fMRI; see Fig. 1 and Supplementary Methods online). The subjects were asked to relax while fixating on the center of the screen where a stream of letters was presented. At some point, when they felt the urge to do so, they were to freely decide between one of two buttons, operated by the left and right index fingers, and press it immediately. In parallel, they should remember the letter presented when their motor decision was consciously made. After subjects pressed their freely chosen response button, a ‘response mapping’ screen with four choices appeared. The subjects indicated when they had made their motor decision by selecting the corresponding letter with a second button press. After a delay, the letter stream started again and a new trial began. The freely paced button presses occurred, on average, 21.6 s after trial onset, thus leaving sufficient time to estimate any potential buildup of a ‘cortical decision’ without contamination by previous trials. Both the left and right response buttons were pressed equally often and most of the intentions (88.6%) were reported to be consciously formed in 1,000ms before the movement (Supplementary Methods and Supplementary Figs. 1–3 online).
We directly assessed how much predictive information each brain region contained about the specific outcome of a motor decision at various time points before and after it reached awareness. For each time point, we measured how much information could be decoded from local patterns of fMRI signals in various brain regions using statistical pattern recognition techniques, 15 (Supplementary Fig. 4 online). These pattern-based decoders were trained to predict the specific outcome of a subject’s motor decision by recognizing characteristic local brain patterns associated with each choice. This highly sensitive approach had several advantages over previous studies. First, it allowed us to investigate any potential long-term determinants of human intentions that preceded the conscious intention far beyond the few hundred milliseconds observed over the SMA1; 14. Second, it allowed us to separately investigate each brain region and determine how much information each region had about the outcome of a motor decision.
Finally, our approach allowed us to identify whether any leading brain activity indeed selectively predicted the outcome of the subject’s choice, rather than reflecting potentially nonspecific preparatory processes. To validate our method, we first investigated which brain regions this decision could be decoded from after it had been made and the subject was executing the motor response. As expected, two brain regions encoded
the outcome of the subject’s motor decision during the execution phase: primary motor cortex and SMA (Fig. 2).
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