Putting thought into action
Introspection leads us to believe that we make decisions and then act upon them, but a recent study shows that the human motor system begins to prepare for action during decision-making as the brain deliberates over the evidence.
HFSP Program Grant holders Daniel Wolpert and Michael Shadlen and colleaguesauthored on Thu, 22 March 2012
The study of decision-making opens a window on the neural basis of higher cognitive capacities. Although we often use our bodies to act upon a decision, common sense tells us that the decision is about a proposition or idea, independent of the method of action that might ensue. A strong version of this view posits a sequential flow of processing (black arrows) from deliberation to decision by the brain’s central executive functions and from decision to action via the motor system, if warranted. Alternatively, if an action is known to ensue based on the outcome of a decision, it may be useful for the motor system to receive a continuous flow of information during deliberation in order to prepare ahead of time, before the decision is made.
A simple form of decision-making arises in the setting of perception under ambiguity, when signals are masked by the presence of noise. For example, the discrimination between two directions of motion in a noisy random dot display invites an analogy to a jury deliberating over the evidence to reach a verdict. For such simple perceptual decisions, much is known about the neural mechanisms underlying evidence accumulation and the rendering of a choice. When a choice is ultimately communicated through an action, say to move the eyes, the evolving decision process has its neural correlate in the firing rates of neurons in areas of the brain that play a role in planning eye movements. These and other findings suggest that at least in highly trained animals the oculomotor system receives a continuous flow of information that could help to prepare an eventual action.
We tested the possibility of continuous flow from decision making to action in humans by using a novel paradigm which allowed us to monitor the movement system before a decision had been reached. Participants made perceptual decisions about random-dot motion direction and indicated their choice by moving a handle to a left or right choice-target. At a random time during motion viewing, we used a robotic device to apply a small rapid perturbation to the arm and measured the muscle stretch reflex. These stretch reflexes reflect the state of the motor system’s gains when it prepares an action, but importantly, we sampled them before the subject had decided on that very action. Nevertheless, we found that the motor system adjusted those gains during decision formation, as the subject accumulated evidence about motion direction. Even more satisfying, the magnitude of the gains increased at the same pace as the evidence accumulated in the decision-maker.
The results resolve a longstanding controversy in cognition: whether perception, ideation, decision-making and action occur in sequential stages or communicate continuously. They support the latter. The motor system can access partial information bearing on a choice before a decision is reached, which helps the motor system prepare. And it suggests that central executive processes, if they exist, do not obstruct this flow.
Deliberation in the Motor System: Reflex Gains Track Evolving Evidence Leading to a Decision. Selen, L. P. J., Shadlen, M. N., & Wolpert, D. M. Journal of Neuroscience, 32(7), 2276–2286 (2012). doi:10.1523/JNEUROSCI.5273-11.2012.