Striatal prediction errors support dynamic control of declarative memory decisions.

Jason M Scimeca,David Badre,Perri L Katzman

doi:10.1038/ncomms13061

Abstract

Adaptive memory requires context-dependent control over how information is retrieved, evaluated and used to guide action, yet the signals that drive adjustments to memory decisions remain unknown. Here we show that prediction errors (PEs) coded by the striatum support control over memory decisions. Human participants completed a recognition memory test that incorporated biased feedback to influence participants' recognition criterion. Using model-based fMRI, we find that PEs—the deviation between the outcome and expected value of a memory decision—correlate with striatal activity and predict individuals' final criterion. Importantly, the striatal PEs are scaled relative to memory strength rather than the expected trial outcome. Follow-up experiments show that the learned recognition criterion transfers to free recall, and targeting biased feedback to experimentally manipulate the magnitude of PEs influences criterion consistent with PEs scaled relative to memory strength. This provides convergent evidence that declarative memory decisions can be regulated via striatally mediated reinforcement learning signals.

Highlights

Adaptive memory requires context-dependent control over how information is retrieved, evaluated and used to guide action, yet the signals that drive adjustments to memory decisions remain unknown
When we included memory strength (MS)-expected value (EV) and expected response outcome (ERO)-EV in the same analysis (GLM 4; see Methods; Supplementary Fig. 3; Supplementary Table 2), we found that the unique variance of these regressors was represented in overlapping areas of ventromedial prefrontal cortex (PFC) and precuneus[38]
We provide convergent evidence that memory control strategies can be learned through reinforcement learning (RL) mechanisms that rely on EV and prediction errors (PEs) signals deriving from memory retrieval itself

Summary

Introduction

Adaptive memory requires context-dependent control over how information is retrieved, evaluated and used to guide action, yet the signals that drive adjustments to memory decisions remain unknown. Follow-up experiments show that the learned recognition criterion transfers to free recall, and targeting biased feedback to experimentally manipulate the magnitude of PEs influences criterion consistent with PEs scaled relative to memory strength This provides convergent evidence that declarative memory decisions can be regulated via striatally mediated reinforcement learning signals. Ventral striatum has been widely associated with receipt of primary and secondary rewards[12,13] as well as reward prediction error (PE), which reflects the degree to which an experienced outcome value deviates from the expected value (EV) Across many experiments, these striatal value signals have been shown to drive learning of cognitive control for action selection and nondeclarative learning[12,14,15,16,17]. Criterion setting is a form of mnemonic control in that it relates retrieved evidence to a context-dependent decision and response

Methods

Results

Conclusion