Calculating the cost of acting in frontal cortex

Abstract

To make informed and successful decisions, it is vital to be able to evaluate whether the expected benefits of a course of action make it worth tolerating the costs incurred to obtain them. The frontal lobe has been implicated in several aspects of goal-directed action selection, social interaction, and optimal choice behavior. However, its exact contribution has remained elusive. Here, we discuss a series of studies in rats and primates examining the effect of discrete lesions on different aspects of cost-benefit decision making. Rats with excitotoxic lesions of the anterior cingulate cortex became less willing to invest effort for reward but showed no change when having to tolerate delays. Orbitofrontal cortex-lesioned rats, by contrast, became more impulsive, yet were just as prepared as normal animals to expend energy to obtain reward. The sulcal region of primate anterior cingulate cortex was also shown to be essential for dynamically integrating over time the recent history of choices and outcomes. Selecting a particular course of action may also come at the expense of gathering important information about other individuals. Evaluating social information when deciding whether to respond was demonstrated to be a function of the anterior cingulate gyrus. Taken together, this indicates that there may be dissociable pathways in the frontal lobe for managing different types of response cost and for gathering social information.

Figure 1

(A) Representation of ACC and OFC regions in the rat brain that were lesioned in the study by Rudebeck and colleagues . ACC includes pre- and perigenual Cg1 and Cg2 and dorsal ACC (ACd). OFC includes medial (MO), ventral (VO) and lateral orbital regions (latter not depicted). (B) Choice performance of ACC- and OFC-lesioned animals and controls in two pre-operative and a single post-operative testing session of the effort-based decision making task. In each block, rats chose between climbing a 30 cm barrier for the HR (4 food pellets) or selecting the unoccupied arm for the LR (2 pellets) (denoted on the figure as “1 × 30cm Barrier”). Adapted from Rudebeck et al. .

Figure 2

Choice performance of ACC- and OFC-lesioned animals and controls in two pre- operative and a single post-operative testing session of the delay-based decision making task. In each block, rats chose between an immediately available LR (1 pellet) or waiting for 15sec for the HR (10 pellets) (denoted on the figure as “1 × 15s Delay”). Adapted from Rudebeck et al. .

Figure 3

Post-operative choice performance of ACC- and OFC-lesioned animals and controls in the equal cost condition (“2 × 30cm Barrier” or “2 × 15s Delay”) and a re-test of the original cost-benefit choice contingency on either (A) the effort-based (“1 × 30cm Barrier”) or (B) delay-based decision making task (“1 × 20s Delay”). Adapted from Rudebeck et al. .

Figure 4

(A)Schematic of the location of the ACCs lesion. (B) Number of trials required to reach and sustain performance within 97% of the optimal rate when the outcome for each choice was probabilistic. Control and ACCs lesion data are shown by white and grey bars respectively. All data come from the post-operative testing period. The optimal rate was defined as $$r_{\mathit{opt}}=\frac{p-\mathit{pq}}{p+q-2\mathit{pq}}$$ where p and q are the probabilities of a new reward being assigned to the lift or turn responses respectively. (C) Number of trials required to reach and sustain performance within 97% of the optimal rate when the outcome for each choice was deterministic. Adapted from Kennerley et al. .

Figure 5

Response latencies to pick up a food item in the presence of either a social stimulus (5 left-hand columns) or two neutral stimuli (2 right-hand columns). Symbols indicate scores for each individual. Redrawn, based on Rudebeck et al..