Errors recruit both cognitive and emotional monitoring systems: Simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI

Abstract

We studied error monitoring in a human patient with unique implantation of depth electrodes in both the left dorsal cingulate gyrus and medial temporal lobe prior to surgery. The patient performed a speeded go/nogo task and made a substantial number of commission errors (false alarms). As predicted, intracranial Local Field Potentials (iLFPs) in dorsal anterior cingulate indexed the detection of errors, showing an early differential activity around motor execution for false alarms, relative to correct responses (either hits or correct inhibitions). More surprisingly, we found that the left amygdala also participated to error monitoring (although no emotional stimuli were used), but with a very different neurophysiological profile as compared with the dorsal cingulate cortex. Amygdala iLFPs showed a precise and reproducible temporal unfolding, characterized by an early monophasic response for correct hits around motor execution, which was delayed by ∼300ms for errors (even though actual RTs were almost identical in these two conditions). Moreover, time-frequency analyses demonstrated a reliable and transient coupling in the theta band around motor execution between these two distant regions. Additional fMRI investigation in the same patient confirmed a differential involvement of the dorsal cingulate cortex vs. amygdala in error monitoring during this go/nogo task. Finally, these intracranial results for the left amygdala were replicated in a second patient with intracranial electrodes in the right amygdala. Altogether, these results suggest that the amygdala may register the motivational significance of motor actions on a trial-by-trial basis, while the dorsal anterior cingulate cortex may provide signals concerning failures of cognitive control and behavioral adjustment. More generally, these data shed new light on neural mechanisms underlying self-monitoring by showing that even “simple” motor actions recruit not only executive cognitive processes (in dorsal cingulate) but also affective processes (in amygdala).