Brain responses to success and failure: Direct recordings from human cerebral cortex

Evaluating the outcome of our own actions is a fundamental process by which we adapt our behavior in our interaction with the external world. fMRI and electrophysiological studies in monkeys have found feedback-specific responses in several brain regions, unveiling facets of a large-scale network predominantly distributed in the frontal lobes. However, a consensus has yet to be reached regarding the exact contribution of each region. The present study benefited from intracerebral EEG recordings in epileptic patients to record directly the neural activity in each of those frontal structures in response to positive and negative feedback. Both types of feedback induced a sequence of high-frequency responses (>40 Hz) in a widespread network involving medial frontal cortex, dorsolateral prefrontal cortex (DLPFC), orbitofrontal cortex (OFC), and insular cortex. The pre-supplementary motor area (pre-SMA), DLPFC, and lateral OFC showed higher activation in response to negative feedback, while medial OFC and dorsal anterior cingulate cortex (dACC) were more responsive to positive feedback. Responses in the medial prefrontal cortex (pre-SMA and dACC) were sustained (lasting more than 1,000 ms), while responses in the DLPFC, insula, and the OFC were short lasting (less than 800 ms). Taken together, our findings show that evaluating the outcome of our actions triggers gamma-range activity modulations in several frontal and insular regions. Moreover, we found that the timing and amplitude of those gamma-band responses reveal fine-scale dissociations between the neural dynamics of positive versus negative feedback processing.