Feature Specific Prediction Errors and Surprise across Macaque Fronto-Striatal Circuits during Attention and Learning

Abstract

Prediction errors signal unexpected outcomes indicating that expectations need to be adjusted. For adjusting expectations efficiently prediction errors need to be associated with the precise features that gave rise to the unexpected outcome. For many visual tasks this credit assignment proceeds in a multidimensional feature space that makes it ambiguous which object defining features are relevant. Here, we report of a potential solution by showing that neurons in all areas of the medial and lateral fronto-striatal networks encode prediction errors that are specific to separate features of attended multidimensional stimuli, with the most ubiquitous prediction error occurring for the reward relevant features. These feature specific prediction error signals (1) are different from a non-specific prediction error signal, (2) arise earliest in the anterior cingulate cortex and later in lateral prefrontal cortex, caudate and ventral striatum, and (3) contribute to feature-based stimulus selection after learning. These findings provide strong evidence for a widely-distributed feature-based eligibility trace that can be used to update synaptic weights for improved feature-based attention.\n\nHighlightsO_LINeural reward prediction errors carry information for updating feature-based attention in all areas of the fronto-striatal network.\nC_LIO_LIFeature specific neural prediction errors emerge earliest in anterior cingulate cortex and later in lateral prefrontal cortex.\nC_LIO_LIVentral striatum neurons encode feature specific surprise strongest for the goal-relevant feature.\nC_LIO_LINeurons encoding feature-specific prediction errors contribute to attentional selection after learning.\nC_LI