Modulation of memory consolidation by the basolateral amygdala or nucleus accumbens shell requires concurrent dopamine receptor activation in both brain regions

Abstract

Previous findings indicate that the basolateral amygdala (BLA) and the nucleus accumbens (NAc) interact in influencing memory consolidation. The current study investigated whether this interaction requires concurrent dopamine (DA) receptor activation in both brain regions. Unilateral, right-side cannulae were implanted into the BLA and the ipsilateral NAc shell or core in male Sprague-Dawley rats ( approximately 300 g). One week later, the rats were trained on an inhibitory avoidance (IA) task and, 48 h later, they were tested for retention. Drugs were infused into the BLA and NAc shell or core immediately after training. Post-training intra-BLA infusions of DA enhanced retention, as assessed by latencies to enter the shock compartment on the retention test. Infusions of the general DA receptor antagonist cis-Flupenthixol (Flu) into the NAc shell (but not the core) blocked the memory enhancement induced by the BLA infusions of DA. In the reverse experiment, post-training intra-NAc shell infusions of DA enhanced retention and Flu infusions into the BLA blocked the enhancement. These findings indicate that BLA modulation of memory consolidation requires concurrent DA receptor activation in the NAc shell but not the core. Similarly, NAc shell modulation of memory consolidation requires concurrent DA receptor activation in the BLA. Together with previous findings, these results suggest that the dopaminergic innervation of the BLA and NAc shell is critically involved in the modulation of memory consolidation.

Figure 1.

(A) Diagram of rat basolateral amygdala (BLA) and adjacent structures (Paxinos and Watson 1997; 2.8 mm posterior to Bregma). (B) Representative photomicrograph of needle track terminating in the BLA. Only data from animals that had needle tracks terminating in the BLA and had no lesions in the surrounding BLA tissue were included in the analyses. (C) Diagram of rat nucleus accumbens (NAc) shell and core and adjacent structures (Paxinos and Watson 2005; 1.8 mm anterior to Bregma). (D) Representative photomicrograph of needle track terminating in the NAc shell. Only data from animals that had needle tracks terminating in the NAc shell and had no lesions in the surrounding NAc tissue were included in the analyses. (E) Representative photomicrograph of needle track terminating in the NAc core. Only data from animals that had needle tracks terminating in the NAc core and had no lesions in the surrounding NAc tissue were included in the analyses. (F) Diagrams of rat brain sections (Paxinos and Watson 2005; 2.16 mm, 2.52 mm, 2.92 mm, and 3.24 mm posterior to Bregma) showing 40 infusion needle termination sites in the BLA (20 from rats with shell cannulations and 20 from rats with core cannulations), as indicated by asterisks, randomly selected from rats included in the final analysis. (G) Diagrams of rat brain sections (Paxinos and Watson 2005; 2.28 mm, 1.92 mm, and 1.56 mm anterior to Bregma) showing the NAc shell and core infusion needle termination sites, as indicated by asterisks, corresponding to the same animals included in F. All diagrams of rat brain sections were adapted with permission from Elsevier © 2005, Paxinos and Watson 2005.

Figure 2.

(A) Retention of rats given either vehicle or DA (3 μg or 10 μg) into the BLA and either vehicle or Flu (10 μg) into the NAc shell immediately after training. Mean latencies, in sec, (±SEM) to enter the shock compartment during the retention test. Groups (from left to right): Vehicle-vehicle (white bar, n = 10); Vehicle-DA (3 μg) (hatched bar, n = 9); vehicle-DA (10 μg), (black bar, n = 8); Flu-vehicle (white bar, n = 6); Flu-DA (3 μg) (hatched bar, n = 9); and Flu-DA (10 μg) (black bar, n = 8). Bars represent mean latencies, in seconds, (±SEM) to enter the shock compartment during the retention test. ^*p < 0.001 compared with vehicle-vehicle and Flu-DA (3 μg). #p < 0.01 compared with vehicle-vehicle and Flu-DA (10 μg). (B) Retention of rats given either vehicle or DA (3 μg or 10 μg) into the BLA and either vehicle or Flu (10 μg) into the NAc core immediately after training. Mean latencies, in sec, (±SEM) to enter the shock compartment during the retention test. Groups (from left to right): Vehicle-vehicle (white bar, n = 12), Vehicle-DA (3 μg) (hatched bar, n = 13), vehicle-DA (10 μg), (black bar, n = 14), Flu-vehicle (white bar, n = 16), Flu-DA (3 μg) (hatched bar, n = 11), and Flu-DA (10 μg) (black bar, n = 11). Bars represent mean latencies, in sec, (±SEM) to enter the shock compartment during the retention test. ^*p < 0.05 compared with vehicle-vehicle. #p < 0.085 compared with Flu-vehicle.

Figure 3.

Retention of rats given either vehicle or DA (4.5 μg or 15 μg) into the NAc shell and either vehicle or Flu (10 μg) into the BLA immediately after training. Mean latencies, in sec, (±SEM) to enter the shock compartment during the retention test. Groups (from left to right): Vehicle-vehicle (white bar, n = 13), vehicle-DA (4.5 μg) (hatched bar, n = 12), vehicle-DA (15 μg), (black bar, n = 9), Flu-vehicle (white bar, n = 6), Flu-DA (4.5 μg) (hatched bar, n = 6), and Flu-DA (15 μg) (black bar, n = 9). Bars represent mean latencies, in sec, (±SEM) to enter the shock compartment during the retention test. ^*p < 0.005 compared with vehicle-vehicle and Flu-DA (15 μg).