Evidence of action sequence chunking in goal-directed instrumental conditioning and its dependence on the dorsomedial prefrontal cortex

Abstract

The current study investigated the contribution of the dorsomedial prefrontal cortex (dmPFC) to instrumental action selection. We found that cell body lesions of the dmPFC, centered on the medial agranular area, spared rats' ability to choose between actions based on either the value or the discriminative stimulus properties of an outcome. We next examined the effects of these lesions on action sequence learning using a concurrent bidirectional heterogeneous chain task in which the identity of the reward delivered was determined by the order in which the two lever press actions were performed. Although both lesioned rats and sham controls learned to perform the task, we found that they relied on different behavioral strategies to do so. In subsequent tests, rats in the sham group were able to withhold their performance of a sequence when either its associated outcome was devalued or the contingency between that sequence and its outcome was degraded by delivering the outcome noncontingently. Interestingly, lesioned rats failed to reorganize their performance at the action sequence level and, rather, were found to withhold their performance of the terminal response in the sequence that had earned the devalued outcome relative to the more distal response, suggesting that they represented the elements of the sequence as distinct behavioral units. These findings demonstrate that rats can use sequence-level representations, or action chunks, to organize their behavior in a goal-directed manner and indicate that the dmPFC plays a critical role in this process.

Figure 1.

Schematic representations of the smallest (light gray) and largest (dark gray) dmPFC lesions. Numbers refer to distance (mm) relative to bregma.

Figure 2.

Effects of dmPFC lesions on acquisition and performance of the single-lever (nonsequence-based) instrumental conditioning task in experiment 1. A, Experimental design (see Materials and Methods for details). B, Acquisition of lever pressing, plotted as the number of responses performed per minute over successive sessions (±SEM). C, Results from outcome devaluation testing, plotted as the mean number of responses performed per minute for the response that had earned the devalued outcome and the response that had earned the other, nondevalued outcome [error bars represent 1 SE of the difference (SED) between means for the effect of outcome value]. D, Results from instrumental reinstatement testing, plotted as the mean rate of responding (presses per minute) during the 2 min periods before (Pre) and after (Post) each outcome delivery for the response trained with that outcome (Reinst) and the response trained with the other outcome (Other) (error bars represent 1 SED between means for the effect of period, presented separately for each response).

Figure 3.

Acquisition of heterogeneous chain performance across training phases 1–4 in dmPFC- and sham-lesioned rats. A, Performance of sequence R1–R2 and sequence R2–R1 as a percentage of all two-lever press sequences performed (see Materials and Methods for details; ±SEM). B, The mean number of lever presses performed per minute (±SEM), plotted separately for actions R1 and R2. The contingencies that were in place during each of the four training phases are outlined at the bottom of the figure (see Materials and Methods for details).

Figure 4.

Sensitivity of chain performance to outcome devaluation in dmPFC- and sham-lesioned rats. A, The percentage of all two-lever press sequences performed (see Materials and Methods), plotted separately for the sequence that earned the devalued outcome and for the sequence that earned the other, nondevalued outcome [error bars represent 1 SE of the difference (SED) between means for the effect of sequence]. B, The mean number of lever presses performed per minute, plotted separately for the two lever press actions based on whether the action was proximal or distal to the devalued outcome during training (error bars represent 1 SED between means for the effect of lever).

Figure 5.

Sensitivity of chain performance to instrumental contingency degradation in dmPFC- and sham-lesioned rats. A, The percentage of all two-lever press sequences performed (±SEM) (see Materials and Methods), plotted separately for the sequence that earned the freely delivered outcome (Degraded) and the sequence that earned the other outcome (Nondegraded). B, The mean number of lever presses performed per minute (±SEM), plotted separately for the two-lever press actions based on whether the action was proximal or distal to the freely delivered outcome.