Incentive memory: evidence the basolateral amygdala encodes and the insular cortex retrieves outcome values to guide choice between goal-directed actions

Abstract

Choice between goal-directed actions is determined by the relative value of their consequences. Such values are encoded during incentive learning and later retrieved to guide performance. Although the basolateral amygdala (BLA) and the gustatory region of insular cortex (IC) have been implicated in these processes, their relative contribution is still a matter of debate. Here we assessed whether these structures interact during incentive learning and retrieval to guide choice. In these experiments, rats were trained on two actions for distinct outcomes after which one of the two outcomes was devalued by specific satiety immediately before a choice extinction test. We first confirmed that, relative to appropriate controls, outcome devaluation recruited both the BLA and IC based on activation of the immediate early gene Arc; however, we found that infusion of the NMDAr antagonist ifenprodil into the BLA only abolished outcome devaluation when given before devaluation. In contrast, ifenprodil infusion into the IC was effective whether made before devaluation or test. We hypothesized that the BLA encodes and the IC retrieves incentive value for choice and, to test this, developed a novel sequential disconnection procedure. Blocking NMDAr activation unilaterally in the BLA before devaluation and then contralaterally in the IC before test abolished selective devaluation. In contrast, reversing the order of these infusions left devaluation intact. These results confirm that the BLA and IC form a circuit mediating the encoding and retrieval of outcome values, with the BLA encoding and the IC retrieving such values to guide choice.

Figure 1.

Experiment 1. A, Mean (±SEM) lever presses per minute across sessions of instrumental training averaged across the two instrumental actions for rats allocated to group Outcome (■; n = 14), group Chow (□; n = 12) and group No food (○; n = 13). Mean (±SEM) lever presses per minute during the instrumental choice test, shown as a percentage of baseline responding during the final 2 d of instrumental training, for group Outcome (B) and (C) for groups Chow and No food. Rats in group Outcome showed increased lever pressing on the lever associated with the valued outcome (white bar) compared with the lever associated with the devalued outcome (black bar). Rats that received home-cage chow or no food during devaluation pressed equally on both levers.

Figure 2.

Experiment 1. A, Representative photomicrographs of Arc-immunoreactivity (Arc-IR) in the amygdala for groups Outcome (n = 8), Chow (n = 8), and No food (n = 7). B, Areas counted for Arc-IR and delineations used. CeN, Central nucleus of the amygdala; LA, lateral amygdala. C, Mean (±SEM) counts of Arc-IR in the BLA, LA, and CeN for groups Outcome (white bars), Chow (black bars), and No food (striped bars). D, Representative photomicrographs of Arc-IR in the IC for groups Outcome, Chow, and No food. E, Area counted for Arc-IR and delineations used. CPU, Caudate–putamen; rf, rhinal fissure. F, Mean (±SEM) counts of Arc-IR in the IC for groups Outcome (white bars), Chow (black bars), and No food (striped bars).

Figure 3.

Experiment 2. A, B, Instrumental test of specific satiety-induced outcome devaluation. Mean (±SEM) lever presses per minute in the extinction test conducted after selective devaluation of one of the outcomes for rats infused before devaluation (n = 10) (A) and for rats infused before the choice test (n = 8) (B). Responding is shown as a percentage of baseline responding during the final 2 d of instrumental training. White bars represent the lever associated with the valued outcome; black bars, the lever associated with the devalued outcome. C, D, Consumption test of specific satiety-induced devaluation. Mean (±SEM) food consumed for rats infused before prefeeding (C) and for rats infused before the test phase (D). Results are presented separately for consumption of the outcome that was the same as (devalued; black bars) and different from (valued; white bars) that outcome consumed immediately before the test phase. E, Microinfusion cannula placements as verified on Nissl-stained sections for the basolateral amygdala. Sections are based on Paxinos and Watson (1998).

Figure 4.

Experiment 3. A, B, Instrumental test of specific satiety-induced outcome devaluation. Mean (±SEM) lever presses per minute in the extinction test conducted after selective devaluation of one of the outcomes for rats infused before devaluation (n = 9) (A) and for rats infused before the choice test (n = 9) (B). Responding is shown as a percentage of baseline responding during the final 2 d of instrumental training. White bars represent the lever associated with the valued outcome; black bars, the lever associated with the devalued outcome. C, D, Consumption test of specific satiety-induced devaluation. Mean (±SEM) food consumed for rats infused before prefeeding (C) and for rats infused before the test phase (D). Results are presented separately for consumption of the outcome that was the same as (devalued; black bars) and different from (valued; white bars) that outcome consumed immediately before the test phase. E, Microinfusion cannula placements as verified on Nissl-stained sections for the IC. Sections are based on Paxinos and Watson (1998).

Figure 5.

Experiment 4. Microinfusion cannula placements as verified on Nissl-stained sections for the insular cortex (A) and basolateral amygdala (B). Sections are based on Paxinos and Watson (1998).

Figure 6.

Experiment 4. A, Diagram of the sequential disconnection procedure used in Experiment 4 for group BLA → IC (n = 9) and group IC → BLA (n = 10) and the predictions for this experiment. h¹ and h² indicate the ipsilateral pathways between the BLA and IC in each hemisphere. B, Mean (±SEM) lever presses per minute in the extinction test conducted after selective devaluation of one of the outcomes. Responding is shown as a percentage of baseline responding during the final 2 d of instrumental training. C, Mean (±SEM) food consumed during the consummatory test of specific satiety-induced outcome devaluation. Results are presented separately for consumption of the outcome that was the same as (devalued; black bars) and different from (valued; white bars) that outcome consumed immediately before the test phase.