The orbitofrontal cortex as part of a hierarchical neural system mediating choice between two good options

Abstract

Animals rely on environmental cues to identify potential rewards and select the best reward available. The orbitofrontal cortex (OFC) is proposed to encode sensory-specific representations of expected outcome. However, its contribution to the selection of a preferred outcome among different reward options is still unclear. We investigated the effect of transient OFC inactivation (achieved by presession injection of muscimol and baclofen) in a novel two-reward choice task. In discrete trials, rats could choose between a solution of polycose and an equally caloric, but highly preferred, solution of sucrose by visiting one of two liquid dispensers after the presentation of a specific cue signaling the availability of one or both of the solutions. We found that OFC inactivation did not affect outcome preference: rats maintained high preference for sucrose and adapted their behavioral responding when the cue-outcome contingencies were reversed. However, when rats were tested drug-free 24 h after OFC inactivation and reversal learning, memory for the newly learned contingencies was poor. These results suggest a potential conflict between OFC (encoding pre-reversal contingencies) and other brain circuits (encoding the new contingencies). Remarkably, repeating the OFC inactivation before the reversal memory test restored normal behavior, confirming the hypothesis of a dominant impact of OFC on other decision-making circuits. These results indicate that the representations encoded in the OFC, while not essential to the expression of outcome preference, exert hierarchical control on downstream decision-making circuits.

Figure 1.

Two-reward choice task. Trials were initiated by responding at the nose poke. The onset of a cue light inside a reward port signaled that sucrose or polycose, respectively, were available following insertion of the snout in the lit port. These cues were presented either individually or simultaneously. In the latter case, rats could choose between both rewards by visiting one of the two reward ports.

Figure 2.

Reconstruction of infusion sites in the OFC. Numbers indicate distance relative to bregma. Symbols on the coronal sections (adapted from Paxinos and Watson, 1998) indicate injector tips for each rat. For Experiments 1a, 1b, 2a, and 2b, white circles indicate saline injections (Sal groups) and black circles indicate M/B injections (M/B groups). For Experiment 3, location of the injector tips is represented by white circles for the Sal–Sal group, gray squares for M/B–Sal group, gray triangles for Sal–M/B group and black circles for M/B–M/B group.

Figure 3.

Effect of OFC inactivation in the two-reward choice task. A, The effect of OFC inactivation with M/B in the two-reward choice task was tested in a reinforced (Experiment 1a: saline, n = 9; M/B, n = 8) or nonreinforced (Experiment 1b: saline, n = 11; M/B, n = 10) version of task. B, Preference score for reinforced test (±SEM). C, Response accuracy during reinforced test, measured as percentage of correct port entries in response to each individual cue (±SEM). D, Preference score during nonreinforced test (±SEM). E, Cumulative number of trials initiated over time during nonreinforced test, expressed as a percentage of the maximum number of trials (120 trials) allowed in the session (±SEM). *p < 0.05, **p < 0.01, ***p < 0.001. S, Sucrose port; P, polycose port; ns, nonsignificant.

Figure 4.

Effect of OFC inactivation on reversal learning and reversal memory in the two-reward choice task (Experiment 2a). A, Experimental design. The OFC was inactivated on reversal day 1 by presession injections of M/B (n = 8). Saline was injected as a control treatment (n = 9). B, Preference score (±SEM) measured before reversal (pre-reversal; left), during reversal (reversal day 1; middle), and during reversal recall (reversal day 2; right). C, Response accuracy measured pre-reversal (left), on reversal day 1 (middle), and reversal day 2 (right). Accuracy is expressed as the percentage of correct port entries in response to each individual cue. D, Evolution of preference (average of 10-trial bins ± SEM) measured pre-reversal (left), on reversal day 1(middle), and reversal day 2 (right). *p < 0.05, **p < 0.01. S, Sucrose port; P, polycose port; ns, nonsignificant.

Figure 5.

Effect of post-reversal OFC inactivation on reversal memory in the two-reward choice task (Experiment 2b). Injections of saline or M/B were made either before reversal session (saline, n = 8; M/B, n = 9) or immediately after reversal session (saline, n = 10; M/B, n = 10). Inactivation of the OFC before, but not immediately after, reversal learning impaired later reversal memory. *p < 0.05; ns, nonsignificant.

Figure 6.

Effect of repeated OFC inactivation on reversal learning and memory in the two-reward choice task (Experiment 3). A, Experimental design. The OFC was inactivated by presession injections of M/B either before reversal learning (reversal day 1: M/B–Sal, n = 12), reversal recall (reversal day 2; Sal–M/B, n = 11), or before both of these sessions (M/B–M/B, n = 10). As a control treatment, saline was injected before both reversal learning and recall test (Sal–Sal, n = 9). B, Preference score (±SEM) measured before reversal (pre-reversal; left), during reversal (reversal day 1; middle), and during reversal recall (reversal day 2; right). C, Evolution of preference (average of 10-trial bins ± SEM) measured pre-reversal (left), on reversal day 1(middle), and reversal day 2 (right). *p < 0.05, **p < 0.01. #, different from Sal–Sal group (#p < 0.05; ###p < 0.001). S, Sucrose port; P, polycose port; ns, nonsignificant.