Abstract

Flexible decision-making strategies (such as planning) are a key component of adaptive behavior, yet their neural mechanisms have remained resistant to experimental analysis. Theories of planning require prediction and evaluation of potential future rewards, suggesting that reward signals may covertly appear at decision points. To test this idea, we recorded ensembles of ventral striatal neurons on a spatial decision task, in which hippocampal ensembles are known to represent future possibilities at decision points. We found representations of reward which were not only activated at actual reward delivery sites, but also at a high-cost choice point and before error correction. This expectation-of-reward signal at decision points was apparent at both the single cell and the ensemble level, and vanished with behavioral automation. We conclude that ventral striatal representations of reward are more dynamic than suggested by previous reports of reward- and cue-responsive cells, and may provide the necessary signal for evaluation of internally generated possibilities considered during flexible decision-making.

Highlights

  • Flexible decision-making strategies are thought to rely on the processing of information beyond current sensory input (Buckner and Carroll, 2007; Hebb, 1949; Tolman, 1932)

  • Because rats were much more likely to reverse direction when moving to the non-rewarded side than when moving to the correct side, we identified points in the rats’ path where during errors, they reversed direction back towards the idealized path

  • We recorded neuronal activity from ventral striatum on a spatial decision task, and observed that the activity of many neurons with a clear reward response was not restricted to the reward sites alone: such neurons tended to be activated, albeit to a lesser degree, at other locations

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Summary

Introduction

Flexible decision-making strategies are thought to rely on the processing of information beyond current sensory input (Buckner and Carroll, 2007; Hebb, 1949; Tolman, 1932). A process of generating and evaluating possible outcomes before they are experienced has been proposed to support complex behaviors such as sensitivity to reward devaluation and action-outcome contingencies in conditioning experiments (Adams and Dickinson, 1981; Balleine and Dickinson, 1998; Holman, 1975), spatial (place) navigation in rats (Johnson and Redish, 2007; O’Keefe and Nadel, 1978; Tolman, 1948), and problem solving in humans (Miller et al, 1960; Newell and Simon, 1972; Shallice, 1982) Put such theories propose that this flexible“planning”system selects a particular action because it (a) predicts the action’s outcome, and (b) judges the outcome to be desirable (Balleine, 2001; Cardinal et al, 2002; Niv et al, 2006; Redish and Johnson, 2007; Toates, 1986). Such non-local representations could provide a prediction component of flexible decision-making; no suitable evaluative signal has yet been identified

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