Opponency revisited: competition and cooperation between dopamine and serotonin

Abstract

Affective valence lies on a spectrum ranging from punishment to reward. The coding of such spectra in the brain almost always involves opponency between pairs of systems or structures. There is ample evidence for the role of dopamine in the appetitive half of this spectrum, but little agreement about the existence, nature, or role of putative aversive opponents such as serotonin. In this review, we consider the structure of opponency in terms of previous biases about the nature of the decision problems that animals face, the conflicts that may thus arise between Pavlovian and instrumental responses, and an additional spectrum joining invigoration to inhibition. We use this analysis to shed light on aspects of the role of serotonin and its interactions with dopamine.

Figure 1

The affect–effect plot. This shows a version of the affective circumplex (Larsen and Diener, 1992; Knutson and Greer, 2008), replacing the arousal axis with action and inhibition. The top-right quadrant is associated with better-than-expected outcomes and their Pavlovian and instrumental effects in learning, approach, and vigor. The bottom-left quadrant is associated with worse-than-expected outcomes, and their effects in terms of inhibition and fear learning. The other quadrants involve more complex interactions between reward and punishment. The top-left arrow shows the case for actions associated with active avoidance of punishments following a movement of the origin left along the valence axis to reflect the prediction of danger; the bottom-right with actions that should be avoided to prevent the loss of otherwise expected rewards, associated with a movement of the origin right along this axis. Dopamine seems particularly associated with the upper right-hand quadrant and, because of its association with active avoidance, effects associated with moving the origin leftward. In the context of this paper, serotonin's prime association is with inhibition, i.e., negative values of the ordinate; the possibility of opponency is that it is responsible for the whole bottom-left quadrant.