Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions

Abstract

The rat medial frontal cortex (MFC) has been implicated in allowing animals to work harder to receive larger rewards. However, it is unknown what role the individual MFC regions [anterior cingulate cortex (ACC) and prelimbic-infralimbic cortex (PL-IL)] play in such decision making. To investigate this, we trained rats on a T-maze cost-benefit task with two possible courses of action, shown previously to be affected by complete MFC lesions. One response involved climbing a 30 cm barrier to obtain a large quantity of reward (high cost-high reward), whereas the other had a lower energetic demand but also a smaller reward gain (low cost-low reward). Before surgery, all animals preferred to select the high cost-high reward option. However, after excitotoxic ACC lesions, there was a complete reversal of behavior, with the ACC group selecting the low cost-low reward response on nearly every trial. In contrast, both control animals and rats with PL-IL lesions continued to choose to climb the barrier for the larger reward. When the same rats were tested on a delayed match-to-sample paradigm however, it was the PL-IL group that was significantly impaired at learning the response rule, with the performance of ACC rats being comparable with controls. This double dissociation indicates that the ACC is the important region within the MFC when evaluating how much effort to expand for a specific reward.

Figure 1.

Representations of the maximal (gray shading) and minimal (black shading) examples of both the ACC (left) and PL-IL (right) lesions.

Figure 2.

Photomicrographs of coronal sections showing typical cell loss for a representative ACC-lesioned (middle) and PL-IL-lesioned (bottom) animal. The boxed regions in the top panels (brain outlines) are shown at high magnification in the middle and bottom panels. The extent of the lesion is indicated by the black arrowheads. Note that both ACC and PL-IL lesions are complete and separate at sections 2.7 mm anterior to bregma.

Figure 3.

Mean ± SE number of choices per day (maximum of 10) that the ACC, PL-IL, and sham groups selected the HR arm when performing the cost-benefit T-maze task. The left panel represents prelesion performance (block A), and the middle panel represents postlesion performance with a single 30 cm barrier in the HR arm (block B). Data in the right panel correspond to postlesion testing with an identical 30 cm barrier in each goal arm (block C).

Figure 4.

a, Mean ± SE number of sessions required by ACC, PL-IL, and sham groups to achieve a criterion of ≥17 of 20 correct trials across two testing sessions on the DMTS task. Asterisks denote a significant difference between the groups at the p < 0.05 level. b, Pattern of acquisition of the matching rule in all three groups across all 24 testing sessions as measured by the mean number of correct trials in each session. c, Number of errors committed on DMTS divided into three phases: a perseverative phase (score of ≤5 of 20 across 2 test sessions), a response bias phase (scores of between 6 and 10 of 20), and finally, a rule-learning phase (≥11 of 20 to criterion). Asterisks denote a significant difference between the groups at the p < 0.05 level.