Differential cingulate and caudate activation following unexpected nonrewarding stimuli

Abstract

This study examined the effects of varying the predictability of nonrewarding events on behavior and neural activation using a rapid mixed-trial functional magnetic resonance imagery (fMRI) design. Twelve adult subjects were scanned with echo planar imaging during performance of a visual detection task where the probability of events (target and nontarget) varied. This task included expected and unexpected nonrewarding events (expected target, unexpected nontarget, and omission of target) in a design that closely parallels studies of dopamine function and reward processing in the alert monkey. We predicted that activation in dopamine-rich areas of the forebrain would behave like the animal literature shows that dopamine neurons in the midbrain behave. Specifically, we predicted increased activity in these regions when an unexpected event occurred and decreased activity when an expected event was omitted. Two main regions, the anterior cingulate and dorsal striatum, showed this pattern. The response in these regions was distinguished by enhanced anterior cingulate activity following the occurrence of an unexpected event and greater suppression of caudate activity following the omission of an expected event. These results suggest that neural activity within specific dopamine-rich brain regions can be modulated by violations in the expectation of nonrewarding events and that the direction of the modulation depends on the nature of the violations.