Transient inactivation of basolateral amygdala during selective satiation disrupts reinforcer devaluation in rats

Abstract

Basolateral amygdala (BLA) function is critical for flexible, goal-directed behavior, including performance on reinforcer devaluation tasks. Here we tested, in rats, the hypothesis that BLA is critical for conditioned reinforcer devaluation during the period when the primary reinforcer (food) is being devalued (by feeding it to satiety), but not thereafter for guiding behavioral choices. We used a spatially independent task that used two visual cues, each predicting one of two foods. An instrumental action (lever press) was required for reinforcer delivery. After training, rats received BLA or sham lesions, or cannulae implanted in BLA. Under control conditions (sham lesions, saline infusions), devaluation of one food significantly decreased responding to the cue associated with that food, when both cues were presented simultaneously during extinction. BLA lesions impaired this devaluation effect. Transient inactivation of BLA by microinfusion of the γ-aminobutyric acid receptor type A agonist muscimol resulted in an impairment only when BLA was inactivated during satiation. When muscimol was infused after satiation and therefore, BLA was inactivated only during the choice test, rats showed no impairment. Thus, BLA is necessary for registering or updating cues to reflect updated reinforcer values, but not for guiding choices once the value has been updated. Our results are the first to describe the contribution of rat BLA to specific components of reinforcer devaluation and are the first to show impairment in reinforcer devaluation following transient inactivation in the rat.

Figure 1

Experimental timeline for instrumental probes of reinforcer devaluation: A) BLA lesion/sham groups and B) BLA inactivation groups.

Figure 2

Timing of the drug/saline infusions: A. MUS/Saline before satiation, B. MUS/Saline after satiation with no delay, C. MUS/Saline after satiation with 30-minute delay before the probe.

Figure 3

BLA lesion histology. A) All cases are superimposed on drawings of coronal sections, the darker the area, the more overlap across lesions. The numbers represent distance in mm from bregma, and approximately correspond to the appropriate planes of the atlas of Paxinos and Watson (2010). B) A representative photomicrograph from a sham-lesioned rat. C) A representative photomicrograph documenting a BLA lesion. LV - the lateral ventricle, CeA - central nucleus of the amygdala, BLA- basolateral subdivision of the amygdala, EC - external capsule.

Figure 4

BLA lesion disrupts reinforcer devaluation in the instrumental probe A) Cumulative number of lever presses (mean+standard error) across the first nine trials for rats with BLA sham or BLA lesions. Solid bars indicate responses to the cue associated with the non-devalued food (Cue_ND), striped bars indicate responses to the cue associated with the devalued food (Cue_D). *denotes a significant difference (p<0.05) between the responses to Cue_ND and Cue_D for sham lesioned rats. There was no significant difference between responses to Cue_ND and Cue_D for BLA lesioned rats. B) Devaluation index (mean+standard error) for cumulative number of lever presses across the first nine trials for sham and BLA lesions. * denotes a significant difference between groups (p<0/05).

Figure 5

Rats with BLA sham and BLA lesions show normal devaluation in the consummatory probe. A) Amount of food consumed in grams (mean+standard error) following devaluation by selective satiation. Solid bars correspond to the non-devalued food (Food_ND), striped bars correspond to the devalued food (Food_D). *denotes a significant difference (p<0.05) between the amount consumed of the devalued and non devalued food for both sham and BLA lesions groups. B) Devaluation index (mean+standard error) for the consummatory probe. There was no significant difference between groups.

Figure 6

Location of BLA infusions. A) Infusion sites plotted on drawings of coronal sections;×represents a correctly placed injection tip, o represents an incorrectly placed injection tip, rats with incorrect placement were excluded from behavioral analyses. The numbers represent distance in mm from bregma, and approximately correspond to the appropriate planes of the atlas of Paxinos and Watson (2010). B) A representative photomicrograph documenting cannula placement in BLA. MeA - medial nucleus of the amygdala, CeA- central nucleus of the amygdala, BLA-basolateral subdivision of the amygdala.

Figure 7

BLA inactivation before satiation disrupts reinforcer devaluation in the instrumental probe. A) Cumulative number of lever presses (mean+standard error) across the first nine trials for each group. Solid bars indicate responses to the cue associated with the non-devalued food (Cue_ND), striped bars indicate responses to the cue associated with the devalued food (Cue_D). *denotes a significant difference (p<0.05) between the responses to Cue_ND and Cue_D for rats treated with saline in BLA and rats treated with MUS after satiation, either with no delay or with a 30-minute delay before the probe. There was no significant difference between responses to Cue_ND and Cue_D for rats that received a MUS infusion before satiation. B) Devaluation index (mean+standard error) for cumulative number of lever presses across the first nine trials for sham and BLA lesions. * denotes a significant difference between groups. MUS before satiation was significantly different from all the other groups.

Figure 8

BLA inactivation does not disrupt reinforcer devaluation in the consummatory probe. A) Amount of food consumed (mean+standard error) in grams following devaluation by selective satiation. Solid bars indicate the non-devalued food (Food_ND), striped bars indicate the devalued food (Food_D). *denotes a significant difference (p<0.05) between the amount of devalued food and non devalued food consumed for saline and both MUS treated groups. B) Devaluation index (mean+standard error) for the consummatory probe. There was no significant difference between groups.