Lesions of Orbitofrontal Cortex Impair Rats' Differential Outcome Expectancy Learning But Not Conditioned Stimulus-Potentiated Feeding

Abstract

Patients with damage to the orbitofrontal cortex (OFC) display various impairments in cognitive and affective function, including a reduced ability to use information about the consequences of their actions to guide their behavior. In this study, rats with neurotoxic lesions of the OFC failed to use specific expectancies about outcomes to guide their learning of an instrumental discrimination task. In contrast, lesioned rats were unimpaired in a measure of learned motivational function, the potentiation of feeding under conditions of food satiation, by a conditioned stimulus that had been paired with food while the rats were food deprived. Notably, performance of both of these tasks has been shown to depend on the function of the basolateral amygdala (BLA), a region that is richly interconnected with the OFC. Thus, the present results are consistent with the view that the acquisition and use of specific outcome expectancies to guide behavior critically involve a neural system that includes the BLA and the OFC, but they indicate that certain motivational properties acquired by cues on the basis of appetitive learning involve BLA circuitry apart from the OFC.

Learned contextual cue potentiates eating in rats

“…Rats that were previously fed these pellets in the conditioning context under food-deprivation (paired group) consumed significantly more food pellets than the rats that were never fed in the context (the unpaired group) [F(1,20) = 5.013, p < 0.04]). This finding is consistent with previous studies that showed CS-potentiated food consumption with explicit CSs [2][3][4][5][6][7]. In the second test, rats were presented with a familiar food different from the training pellets, standard lab chow.…”

“…For example, an auditory or visual conditioned stimulus (CS) that is paired with a food unconditioned stimulus (US) when rats are food-deprived will stimulate eating when they are food-sated [2]. A number of recent studies identified components of brain circuitry critical to the occurrence of this cue-potentiated eating [3][4][5][6][7]. However, those studies used a single training protocol, and only evaluated consumption of the food used as the US.…”

Differential involvement of the basolateral amygdala, orbitofrontal cortex, and nucleus accumbens core in the acquisition and use of reward expectancies.

“…Similarly, Mc-Dannald et al (2005) examined their data prior to the delivery of the first outcome, and these preoutcome data were similar to those from the entire stimulus duration (there was a DOE effect in shams, but not in rats with OFC lesions). Both of these measures demonstrated that without the direct experience of the outcome, sham animals display the DOE to the S D alone, whereas animals with lesions to either the BLA or OFC do not (see Figure 3 of Blundell et al, 2001, and Figure 4 of McDannald et al, 2005).…”

“…BLA lesions impair performance on appetitive Pavlovian second-order conditioning, reinforcer devaluation (Hatfield, Jan, Conley, Gallagher, & Holland, 1996), conditional discrimination involving the DOE, and reward-specific Pavlovian-to-instrumental transfer (Blundell et al, 2001). The OFC is a cortical region with extensive connections to the BLA as well as other cortical and subcortical regions (hippocampus, basal ganglia, and thalamic nuclei) that may act as the goal-directed correlate of reward expectancy in the presence of a discriminative stimulus (Barbas, 2000;Cardinal et al, 2002;McDannald, Saddoris, Gallagher, & Holland, 2005;Pickens, Saddoris, Gallagher, & Holland, 2004;Schoenbaum, Setlow, Saddoris, & Gallagher, 2003). More specifically, it has been inferred that the OFC specializes in processing features essential for the guidance of behavior based on outcome expectancies (Schoenbaum, Chiba, & Gallagher, 1998).…”

“…In contrast, emerging findings suggest that the BLA and OFC reward circuits are necessary for the production of the reward expectancies produced by the DOP (Blundell et al, 2001;McDannald et al, 2005;Saddoris, McDannald, Gallagher, & Holland, 2004). Collectively, these findings support Savage's claim that altering reward contingency by embedding the DOP (e.g., pairing specific cues with a specific reward condition) into a task alters both the neural system and strategy engaged, as compared with the NOP (Ramirez et al, 2005;Savage, 2001;Savage et al, 1999Savage et al, , 2004.…”