Urgency tunes center-surround inhibition in the primary motor cortex during action selection

Action selection involves a tight balance between the competing demands of decision speed and accuracy. Recent work suggests that this balance is adjusted by an urgency signal which increases during action selection as movement execution draws nearer, and can further intensify depending on context. Interestingly, single-neuron recordings in non-human primates suggest that urgency operates as a global gain modulator, amplifying activity in both decision-related and nondecision-related cells of motor areas when speed is of essence. Here, we investigated the impact of urgency on corticospinal excitability in decision-related and nondecision-related muscles in humans by applying transcranial magnetic stimulation (TMS) over the primary motor cortex. Subjects performed a modified version of the tokens task (Thura and Cisek, 2017, Neuron). In each trial, 15 tokens jumped one-by-one every 200 ms from a central circle to one of two lateral target circles; participants had to guess which of those targets would ultimately receive the majority of the tokens, and to report their decision before the final token jump on a key-board with either the left or the right index finger. Importantly, the reward provided for correct choices was proportional to the number of tokens remaining in the central circle at the time of the response (which decreased over time), increasing the urge to act as time elapsed. Further, we manipulated the overall level of urgency by providing different penalties for incorrect responses in two separate block types. In one block type, the cost of making an error was low, hence further increasing the sense of urgency and encouraging hasty decisions (UrgencyHigh block). In the other block type, the cost of making an error was high, decreasing the overall level of urgency and promoting decision accuracy (UrgencyLow block). We exploited TMS to elicit motor evoked potentials (MEPs) at different timings during the decision process in an index finger muscle (i.e., involved in the response [decision-related muscle]) and in thumb and pinky muscles (i.e., not involved in the response [nondecision-related muscles]). MEP amplitudes provided us with a muscle-specific assay of corticospinal excitability at the time of the stimulation. Our results indicate that urgency tunes corticospinal excitability in opposite ways in decision-related muscles compared to nondecision-related ones. Indeed, MEPs exhibited more facilitation in the UrgencyHigh than in the UrgencyLow blocks in the decision-related muscle when it was selected for the forthcoming movement. Conversely, MEPs showed more suppression in the UrgencyHigh than in the UrgencyLow blocks in the nondecision-related muscles. Hence, urgency concomitantly facilitated corticospinal excitability in a decision-related muscle and inhibited it in nondecision-related, surrounding muscles, boosting action selection through a mechanism reminiscent of center-surround inhibition