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

Abstract

In this study, the authors tested the hypothesis that the basolateral amygdala (BLA), orbitofrontal cortex (OFC), nucleus accumbens core (NA-core), and the extended hippocampus mediate different aspects of the development-maintenance of unique reward expectancies produced by the differential outcomes procedure (DOP). Rats were trained with either DOP or a nondifferential outcomes procedure (NOP) on a simple discrimination task. Fornix lesions did not affect either version of the task, demonstrating that the extended hippocampal system has no role in stimulus-outcome (S-O) associations. In contrast, in the DOP condition, BLA lesions impaired performance throughout training, OFC lesions impaired choice accuracy only in the later maintenance phase, and NA-core lesions resulted in enhanced learning. These results suggest that BLA and OFC are important for establishment (BLA) and behavioral maintenance (OFC) of S-O associations, whereas the NA-core is not needed and can in fact impede using multiple S-O associations. No impairments were observed in the NOP condition, demonstrating that these structures are not critical to stimulus-response learning.

Figure 1

Photomicrographs showing cresyl violet stained sections of representative lesions and a control for comparison (left) and schematic representations (Paxinos & Watson, 1998) of lesion placement (right) of each brain region of interest. Shaded areas represent the maximum (light gray) and minimum (dark gray) extent of the lesions for the animals included in the behavioral analyses. From The Rat Brain in Stereotaxic Coordinates (Figures 5, 7, 9, 10, 12, 14, 15, 22−24, 26, 27, 29, 31, 33), by G. Paxinos and C. Watson, 1998, San Diego, CA: Academic Press. Copyright 1998 by Elsevier. Adapted with permission.

Figure 2

The mean percentage correct and standard error during acquisition and maintenance of a conditional discrimination for (a) sham-lesioned, (b) fornix-lesioned, (c) basolateral amygdala (BLA)-lesioned, (d) orbitofrontal cortex (OFC)-lesioned, and (e) nucleus accumbens (NAc)-lesioned rats trained with the differential outcomes procedure (DOP) or the nondifferential outcomes procedure (NOP). These data are presented across 20 sessions, separated into early learning phase (Session 1−10) and late learning phase (Sessions 11−20).

Figure 3

The mean difference (± SEM) between differential outcomes procedure (DOP) and nondifferential outcomes procedure (NOP) groups accuracy scores (percentage correct DOP – percentage correct NOP) for three time points (early [Session 1], middle [Sessions 8−10], and late [Sessions 18−20]) of the acquisition–maintenance curve for the conditional discrimination task. BLA = basolateral amygdala; OFC = orbitofrontal cortex; NAc = nucleus accumbens core.

Figure 4

The mean number (± SEM) of responses on both the correct and incorrect levers across all sessions (Session 1−20) for subjects from each lesion condition (sham, fornix, basolateral amygdala [BLA], orbito-frontal cortex [OFC], nucleus accumbens core [NAc-core]) trained with either the differential outcomes procedure (DOP) or the nondifferential outcomes procedure (NOP), shown as a log function. These data are divided into early and late learning phases.