While conflict between incompatible goals has well-known effects on actions, in many situations the same action may produce harmful or beneficial consequences during different periods in a nonconflicting manner, e.g., crossing the street during a red or green light. To avoid harm, subjects must be cautious to inhibit the action specifically when it is punished, as in passive avoidance, but act when it is beneficial, as in active avoidance or active approach. In mice of both sexes performing a signaled action to avoid harm or obtain reward, we found that addition of a new rule that punishes the action when it occurs unsignaled delays the timing of the signaled action in an apparent sign of increased caution. Caution depended on task signaling, contingency, and reinforcement type. Interestingly, caution became persistent when the signaled action was avoidance motivated by danger but was only transient when it was approach motivated by reward. Although caution is represented by the activity of neurons in the midbrain, it developed independent of frontal cortex or basal ganglia output circuits. These results indicate that caution disrupts actions in different ways depending on the motivational state and may develop from unforeseen brain circuits.SIGNIFICANCE STATEMENT Actions, such as crossing the street at a light, can have benefits during one light signal (getting somewhere) but can be harmful during a different signal (being run over). Humans must be cautious to cross the street during the period marked by the appropriate signal. In mice performing a signaled action to avoid harm or obtain reward, we found that addition of a new rule that punishes the action when it occurs unsignaled, delays the timing of the signaled action in an apparent sign of increased caution. Caution became persistent when the signaled action was motivated by danger, but not when it was motivated by reward. Moreover, the development of caution did not depend on prototypical frontal cortex circuits.
Keywords: approach; avoidance; basal ganglia; frontal cortex; midbrain.
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