Error monitoring using external feedback: specific roles of the habenular complex, the reward system, and the cingulate motor area revealed by functional magnetic resonance imaging

Abstract

The dopaminergic system has been shown to be involved in the processing of rewarding stimuli, specifically of errors in reward prediction, in animal studies as well as in recent neuroimaging studies in humans. Furthermore, a specific role of dopamine in the human homolog of the rostral cingulate motor area (rCMA) was proposed in a recent model of error detection. Negative feedback as well as self-detected errors elicit a negative event-related brain potential probably generated in the rCMA. We performed two experiments using functional magnetic resonance imaging to investigate the brain activity related to negative and positive feedback in a dynamically adaptive motion prediction task. Whereas positive feedback raised hemodynamic activity in the ventral striatum (nucleus accumbens), negative feedback activated the rCMA, the inferior anterior insula, and the epithalamus (habenular complex). These data demonstrate the role of the habenular complex in the control of the human reward system, a function previously hypothesized on the basis of animal research. The rCMA reacted only to errors with negative feedback but not to errors without feedback, which ruled out an influence of response conflict or uncertainty on its role in error detection by external signals.

Figure 1.

Timing of the dynamically adaptive motion prediction task (“first-over-the-finish-line-task”). Note that the noninformative stimuli instead of feedback were presented only in experiment 2.

Figure 2.

Activation of the epithalamus in experiment 1. a, Overlap area resulting from variability of the habenular complex across subjects. b, z-map of activation. From left to right: coronal, sagittal, and horizontal slices at x = −2, y = −25, and z = 8.

Figure 3.

Activations in experiment 2. The central picture shows the z-map resulting from contrasting negative and positive informative feedback. a–d, Signal change of the hemodynamic response for correct and error trials with and without informative feedback at the CMA (a), pre-SMA (b), habenular complex (c), ventral striatum (nucleus accumbens) (d), and left insula (e).