Medial temporal lobe high-frequency activity at feedback signals error and predicts subsequent memory during spatial learning

Abstract

\n The ability to incorporate information about feedback is critical for associative learning. The medial temporal lobe (MTL) and prefrontal cortex (PFC) are thought to be involved in processing feedback as new associations are learned. However, the relative contributions of these regions to feedback processing and subsequent memory performance in humans are poorly understood. To address this question, we tested pre-surgical epilepsy patients with depth electrodes implanted in the MTL and PFC using a spatial memory task in which subjects learned object-location associations over time. We found increased high-frequency activity (HFA; 40-100 Hz), thought to reflect local excitatory activity, in the MTL and dorsolateral PFC (dlPFC) at feedback for high error trials. In the MTL, this HFA error signal predicted greater trial-by-trial decreases in error from one training block to the next indicating that these signals are involved in updating memory representations or modifying incorrect associations during learning. The opposite pattern of activity was observed during retrieval, with greater MTL and dlPFC HFA predicting lower error, replicating previous results from our group. Overall, these data suggest putative mechanisms for the learning of object-location associations.