Double dissociation of stimulus-value and action-value learning in humans with orbitofrontal or anterior cingulate cortex damage

Abstract

Adaptive decision making involves selecting the most valuable option, typically by taking an action. Such choices require value comparisons, but there is debate about whether these comparisons occur at the level of stimuli (goods-based) value, action-based value, or both. One view is that value processes occur in series, with stimulus value informing action value. However, lesion work in nonhuman primates suggests that these two kinds of choice are dissociable. Here, we examined action-value and stimulus-value learning in humans with focal frontal lobe damage. Orbitofrontal damage disrupted the ability to sustain the correct choice of stimulus, but not of action, after positive feedback, while damage centered on dorsal anterior cingulate cortex led to the opposite deficit. These findings argue that there are distinct, domain-specific mechanisms by which outcome value is applied to guide subsequent decisions, depending on whether the choice is between stimuli or between actions.

Figure 1.

Lesion overlap images superimposed on 3D reconstructions of the MNI brain (top left panel OFC group, top right panel dACC group) and on the same axial slices (middle panel upper row, OFC group; lower row, dACC group). Colors show degree of overlap, as indicated in the legend. The bottom panel shows a representative image for each individual subject, with those in the OFC group on the left, and the dACC group on the right.

Figure 2.

Mean proportion of win–shift behavior by task and group. The frequency of win–shift behavior was calculated by counting the number of response shifts immediately after congruent positive feedback and dividing it by the total number of trials following congruent positive feedback. Error bars indicate SEM. *p < 0.05.