Reward-evoked dopamine transients are well-established as prediction errors. However the central tenet of temporal difference accounts-that similar transients evoked by reward-predictive cues also function as errors-remains untested. Here we addressed this by showing that optogenetically-shunting dopamine activity at the start of a reward-predicting cue prevents secondorder conditioning without affecting blocking. These results indicate that cue-evoked transients function as temporal-difference prediction errors rather than reward predictions.
Behavioral change is paramount to adaptive behavior. Two ways to achieve alterations in previously established behavior are extinction and overexpectation. The infralimbic (IL) portion of the medial prefrontal cortex controls the inhibition of previously established aversive behavioral responses in extinction. The role of the IL cortex in behavioral modification in appetitive Pavlovian associations remains poorly understood. Here, we seek to determine if the IL cortex modulates overexpectation and extinction of reward learning. Using overexpectation or extinction to achieve a reduction in behavior, the present findings uncover a dissociable role for the IL cortex in these paradigms. Pharmacologically inactivating the IL cortex left overexpectation intact. In contrast, pre-training manipulations in the IL cortex prior to extinction facilitated the reduction in conditioned responding but led to a disrupted extinction retrieval on test drug-free. Additional studies confirmed that this effect is restricted to the IL and not dependent on the dorsally-located prelimbic cortex. Together, these results show that the IL cortex underlies extinction but not overexpectation-driven reduction in behavior, which may be due to regulating the expression of conditioned responses influenced by stimulus–response associations rather than stimulus–stimulus associations.
The discovery that DA transients can be mapped onto the reward prediction errors in temporal difference models is a pinnacle achievement of neuroscience. Yet, there is abundant evidence that DA activity reinforces actions, suggesting it serves as an intrinsically rewarding event. These two possibilities are so conceptually intertwined that it is not surprising that they have been so far experimentally conflated. Here, using computational modeling, behavioural blocking and optogenetics, we show that stimulating VTA DA neurons promotes learning even when a natural reward and DA stimulation are held constant across the learning phases of blocking. These findings provide strong evidence in favour of the prediction error hypothesis rather than encoding the rewarding value of appetitive events.
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