Enhanced inter-regional coupling of neural responses and repetition suppression provide separate contributions to long-term behavioral priming

Stephen J Gotts,Shawn C Milleville,Alex Martin

doi:10.1038/s42003-021-02002-7

Stephen J Gotts, Shawn C Milleville + Show 1 more

Open Access

https://doi.org/10.1038/s42003-021-02002-7

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Abstract

Stimulus 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 data were most consistent with the Synchrony model, with increased coupling between right temporoparietal and anterior cingulate cortex for repeated objects that correlated with priming magnitude across participants. Increased coupling and repetition suppression varied independently, each explaining unique variance in priming and requiring modifications of all current models.

Highlights

Stimulus identification commonly improves with repetition over long delays (“repetition priming”), whereas neural activity commonly decreases (“repetition suppression”)
At a minimum level of significance (P < 0.05, q < 0.05), most of the voxels responding above baseline exhibited repetition suppression, with more restricted locations showing repetition enhancement, including cingulate cortex just dorsal to the posterior portion of the corpus callosum, bilateral cuneus, right posterior superior temporal gyrus (STG), and bilateral putamen
In a recent study of short-term priming in picture naming using electrocorticography (ECoG), we found evidence of both earlier neural response onset consistent with the Facilitation model, as well as increased top-down effective connectivity from left frontal cortex to left ventral temporal cortex with repetition within the first 200 milliseconds of processing[43], potentially consistent with the Predictive Coding model

Summary

Introduction

Stimulus identification commonly improves with repetition over long delays (“repetition priming”), whereas neural activity commonly decreases (“repetition suppression”). Bottom-up support would be removed for alternative or competing representations in downstream brain regions, allowing more rapid propagation of stimulus-selective activity throughout task-engaged neural pathways, as well as faster and more accurate behavioral responses While these models are not necessarily mutually exclusive, each makes unique predictions that can be tested. The ability of BOLD fMRI to adjudicate subtle changes in the timing of neural activity is less clear, but we examine the predicted timing changes of the Facilitation and Predictive Coding models in the event that relevant timing information is detectable What this means is that it will not be possible to test all four models on equal terms, but the results will have the potential to favor certain models over others, as well as to clarify the relationships between changes in connectivity, repetition suppression, and representational similarity

Results

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