The contribution of ventrolateral and dorsolateral prefrontal cortex to response reversal

Abstract

Studies investigating response reversal consistently implicate regions of medial and lateral prefrontal cortex when reinforcement contingencies change. However, it is unclear from these studies how these regions give rise to the individual components of response reversal, such as reinforcement value encoding, response inhibition, and response change. Here we report a novel instrumental learning task designed to determine whether regions implicated in processing reversal errors are uniquely involved in this process, or whether they play a more general role in representing response competition, reinforcement value, or punishment value in the absence of demands for response change. In line with previous findings, reversal errors activated orbitofrontal cortex, dorsomedial prefrontal cortex, ventrolateral prefrontal cortex, caudate, and dorsolateral prefrontal cortex. These regions also showed increased activity to errors in the absence of contingency changes. In addition, ventrolateral PFC, caudate, and dorsolateral PFC each exhibited increased activity following correct reversals. Activity in these regions was not significantly modulated by changes in reinforcement value that were not sufficient to make an alternative response advantageous. These data do not support punishment-processing or prepotent response inhibition accounts of ventrolateral prefrontal cortex function. Instead, they support recent conceptualizations of ventrolateral prefrontal cortex function that implicate this region in resolving response competition by manipulating the representation of either motor response options, or object features. These data also suggest that dorsolateral prefrontal cortex plays a role in reversal learning, probably through top down attentional control of object or reinforcement features when task demands increase.

Figure 1

The stock market task. One distinct stimulus type is shown. The “cheese” stock undergoes a change in value that makes response change advantageous (depicted in a-d). Each row represents a separate sample trial. a) Correct acquisition trial. Left: The response option screen shows the stock (cheese), and the current market value of the stock “Sell this stock now and lose $75.” Next to the current market value is the alternate response option: “Keep this stock and see if it grows.” In this case, the participant elected to keep the stock. Right: The feedback screen. Here the subject gained $50 instead of losing $75 as indicated by the updated red boxes, which show the value of the response just made (“By keeping this stock, you gained $50”), as well as the value of the forgone response (“You would have lost $75”). b) Acquisition error. Left: The subject chooses to sell the stock now and lose $75. Right: The feedback screen indicates that selling the stock cost the subject $75 whereas they would have gained $50 had they kept the stock. c) Reversal error. This sample depicts a stimulus that changes in valence of reinforcement and best response. Left: The subject chooses to keep the stock. However, this stimulus has undergone a reversal. Right: The feedback screen indicates that while selling the stock still costs the subject $75, keeping the stock now costs even more ($100). So in the reinforcement shift phase, this stimulus underwent a change of valence and best response (the value of keeping the stock went from a gain of $50 to a loss of $100 and the best response changed from keeping the stock to selling it). d) Correct reversal. Left: The subject now chooses to sell the stock. Right: The feedback screen reflects that the subject received a loss of only $75 by selling the stock versus the $100 loss that would have resulted from keeping it.

Figure 2

Images depicting significant activation in dorsomedial PFC, ventrolateral PFC, and caudate elicited by the contrast response reversal errors versus the control condition (p < 0.001, and p < 0.01 corrected). The conditions are abbreviated as follows: correct acquisition (Aq), correct control (Con), correct value change (VC), correct reversals (Rev), acquisition errors (AqErr), non-reversal errors (NRErr) and reversal errors (RevErr).

Figure 3

The graph depict the percent signal change across conditions within the region of dorsolateral prefrontal cortex shown.