Enhanced inter-regional coupling of neural responses underlies long-term behavioral priming

Abstract

SummaryStimulus identification commonly improves with repetition over long delays (“repetition priming”), whereas neural activity commonly decreases (“repetition suppression”). Multiple models have been proposed to explain this brain-behavior relationship, predicting alterations in functional and/or effective connectivity (Synchrony and Predictive Coding models), in the latency of neural responses (Facilitation model), and in the relative similarity of neural representations (Sharpening model). Here, we test these predictions with fMRI during overt and covert naming of repeated and novel objects. While we find partial support for predictions of the Facilitation and Sharpening models in the left fusiform gyrus and left frontal cortex, the strongest support was observed for the Synchrony model, with increased coupling between right temporoparietal and anterior cingulate cortex for repeated objects that correlated with priming magnitude across participants. Despite overlap with regions showing repetition suppression, increased coupling and repetition suppression varied independently, establishing that they follow from distinct mechanisms.HighlightsTested four prominent neural models of repetition suppression and long-term primingConnectivity analyses supported Synchrony model but not Predictive Coding modelTiming, spatial similarity of responses partially support Facilitation, SharpeningRepetition suppression was independent of coupling, implying distinct mechanismseTOCGotts et al. test four prominent neural models of repetition suppression and behavioral priming. They show that the model with the most support is the Synchrony model: a whole-brain connectivity analysis revealed that temporoparietal cortex has increased coupling with anterior cingulate cortex following repetition, particularly for strongly primed objects.