Dopamine signals encode internal reward value rather than externally indicated attributes

Abstract

Abstract The dopamine reward prediction error signal is known to be subjective but has so far only been related to explicit external stimuli and rewards. However, personal choices are based on private internal values of the rewards at stake. Without indications of an agent’s private internal value, we do not know whether dopamine neurons, or any reward neurons, encode the internal value. The well-established Becker-DeGroot-Marschak (BDM) auction-like mechanism allows participants to place bids for freely stating their private internal value for a good. BDM bids are known to reflect the agent’s true internal valuation, as inaccurate bidding results in suboptimal reward (‘incentive compatibility’). In our experiment rhesus monkeys placed BDM bids for juice rewards without specific external constraints. Their bids for physically identical rewards varied trial by trial and increased overall for larger rewards. Responses of midbrain dopamine neurons followed the trial-by-trial variation of bids despite constant, explicitly predicted reward amounts; correspondingly, the dopamine responses were similar when the animal placed similar bids for different reward amounts. Support Vector Regression demonstrated accurate prediction of the animal’s bids by as few as twenty dopamine neurons, demonstrating the validity of the dopamine code for internal reward value. Thus, dopamine responses reflect the instantaneous internal subjective reward value rather than the value imposed by external stimuli.