Midbrain dopamine neurons provide teaching signals for goal-directed navigation

In naturalistic environments, animals navigate in order to harvest rewards. Successful goal-directed navigation requires learning to accurately estimate location and select optimal state-dependent actions. Midbrain dopamine neurons are known to be involved in reward value learning1-13. They have also been linked to reward location learning, as they play causal roles in place preference14,15 and enhance spatial memory16-21. Dopamine neurons are therefore ideally placed to provide teaching signals for goal-directed navigation. To test this, we imaged dopamine neural activity as mice learned to navigate in a closed-loop virtual reality corridor and lick to report the reward location. Across learning, phasic dopamine responses developed to visual cues and trial outcome that resembled reward prediction errors and indicated the animals estimate of the reward location. We also observed the development of pre-reward ramping activity, the slope of which was modulated by both learning stage and task engagement. The slope of the dopamine ramp was correlated with the accuracy of licks in the next trial, suggesting that the ramp sculpted accurate location-specific action during navigation. Our results indicate that midbrain dopamine neurons, through both their phasic and ramping activity, provide teaching signals for improving goal-directed navigation. HighlightsO_LIWe investigated midbrain dopamine activity in mice learning a goal-directed navigation task in virtual reality C_LIO_LIPhasic dopamine signals reflected prediction errors with respect to subjective estimate of reward location C_LIO_LIA slow ramp in dopamine activity leading up to reward location developed over learning and was enhanced with task engagement C_LIO_LIPositive ramp slopes were followed by improved performance on subsequent trials, suggesting a teaching role during goal-directed navigation C_LI