Functional Connectivity between Amygdala and Cingulate Cortex for Adaptive Aversive Learning

•Neurons representing signed and absolute errors exist in the amygdala and dACC•Amygdala neurons signal more absolute errors and negative outcome•Absolute errors in the amygdala precede dACC during successful learning•dACC activity precedes development of signed errors in the amygdala

SummaryThe ability to switch flexibly between aversive and neutral behaviors based on predictive cues relies on learning driven by surprise or errors in outcome prediction. Surprise can occur as absolute value of the error (unsigned error) or its direction (signed errors; positive when something unexpected is delivered and negative when something expected is omitted). Signed and unsigned errors coexist in the brain and were associated with different systems, but how they interact and form across large networks remains vague. We recorded simultaneously in the amygdala and dorsal anterior cingulate cortex (dACC) of monkeys performing a reversal aversive-conditioning paradigm and quantified changes in interregional correlations when contingencies shift. We report that errors exist in different magnitudes and that they differentially develop at millisecond resolution. Our results support a model where unsigned errors first develop in the amygdala during successful learning and then propagate into the dACC, where signed errors develop and are distributed back to the amygdala.