Brain mechanisms for switching from automatic to controlled eye movements

Human behaviour is mostly composed of habitual actions that require little conscious control. Such actions may become invalid if the environment changes, at which point we need to switch behaviour by overcoming habitual actions that are otherwise triggered automatically. It is unclear how the brain controls this type of behavioural switching. Here we show that the presupplementary motor area (pre-SMA) in the medial frontal cortex has a function in switching from automatic to volitionally controlled action. This was demonstrated using colour-matching saccade tasks performed by rhesus monkeys. We found that a group of pre-SMA neurons was selectively activated when subjects successfully switched from a habitual saccade to a controlled alternative saccade. Electrical stimulation in the pre-SMA replaced automatic incorrect saccades with slower correct saccades. A further test suggested that the pre-SMA enabled switching by first suppressing an automatic unwanted saccade and then boosting a controlled desired saccade. Our data suggest that the pre-SMA resolves response conflict so that the desired action can be selected. Possible neuronal circuits through which the pre-SMA might exert its switching functions will be discussed.