Rewarding Value or Prediction Error: Settling the debate over the role of dopamine in reward learning

Abstract

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.

A disengaging property of medial accumbens shell dopamine

“…Operant responses for stimulation of dopamine neurons creates an error such that the receipt of stimulation is better than expected, and the response is repeated with increasing vigour. Attempts have been made to disentangle the hypotheses that optogenetic stimulation of ventral tegmental area dopamine neurons acts as a reinforcer or error signal [15,24], but these procedures overlook separable roles of dopamine neurons with distinct striatal targets [25][26][27]. Notably, dopamine activity in the medial accumbens shell is inconsistent with error coding [28], modulated by the value of natural taste stimuli [29], and directly supports self-stimulation [27], highlighting a role for this substrate as a reinforcer.…”