Dissociable roles for the basolateral amygdala and orbitofrontal cortex in decision-making under risk of punishment

Abstract

Several neuropsychiatric disorders are associated with abnormal decision-making involving risk of punishment, but the neural basis of this association remains poorly understood. Altered activity in brain systems including the basolateral amygdala (BLA) and orbitofrontal cortex (OFC) can accompany these same disorders, and these structures are implicated in some forms of decision-making. The current study investigated the role of the BLA and OFC in decision-making under risk of explicit punishment. Rats were trained in the risky decision-making task (RDT), in which they chose between two levers, one that delivered a small safe reward, and the other that delivered a large reward accompanied by varying risks of footshock punishment. Following training, they received sham or neurotoxic lesions of BLA or OFC, followed by RDT retesting. BLA lesions increased choice of the large risky reward (greater risk-taking) compared to both prelesion performance and sham controls. When reward magnitudes were equated, both BLA lesion and control groups shifted their choice to the safe (no shock) reward lever, indicating that the lesions did not impair punishment sensitivity. In contrast to BLA lesions, OFC lesions significantly decreased risk-taking compared with sham controls, but did not impair discrimination between different reward magnitudes or alter baseline levels of anxiety. Finally, neither lesion significantly affected food-motivated lever pressing under various fixed ratio schedules, indicating that lesion-induced alterations in risk-taking were not secondary to changes in appetitive motivation. Together, these findings indicate distinct roles for the BLA and OFC in decision-making under risk of explicit punishment.

Keywords: addiction; amygdala; decision-making; orbitofrontal cortex; punishment; risk.

Figure 1.

Representative histology from rats that received either neurotoxic or sham lesions of the basolateral amygdala. A, The extent of neurotoxic lesions of the basolateral amygdala is depicted schematically, with the maximum lesion extent (gray) and minimum lesion extent (black) indicated in both hemispheres. B, Representative thionin-stained coronal images of the basolateral amygdala in a lesioned rat and a sham rat are displayed. Images were taken using a 250× objective lens.

Figure 2.

Choice performance on the risky decision-making task before and after basolateral amygdala lesions. A, Before surgery, there was no difference in choice of the large risky reward between the groups that would go on to receive lesion or sham surgeries. B, After surgery, the lesion group (n = 18) showed a significant increase in choice of the large risky reward compared with both presurgery baseline and postsurgery sham controls (n = 15). Data (mean ± SEM percentage choice of the large risky reward) are averaged over the final five sessions (both before and after surgery), at which point rats displayed stable performance.

Figure 3.

Response latencies in the risky decision-making task before and after basolateral amygdala lesions. A, Before surgery, both groups had significantly longer latencies to respond on the lever associated with the large risky reward compared with the lever associated with the small safe reward. B, After surgery, the lesion group (n = 18) had significantly longer latencies to respond on the small reward lever compared to their pre-surgical performance, but significantly shorter latencies to respond on the large reward lever compared to both pre-surgical performance and sham controls (n = 15). Data (mean ± SEM seconds) are averaged over the final five sessions (both before and after surgery), at which point rats displayed stable performance.

Figure 4.

Performance in the risky decision-making task when reward magnitudes were equated. Both lesion (n = 11) and sham (n = 4) groups shifted their choices to the nonshock-associated (safe) lever to the same degree. Data (mean ± SEM percentage choice of the risky reward) are from the final five sessions of testing, at which point rats displayed stable performance.

Figure 5.

Effects of amphetamine on the risky decision-making task in rats with basolateral amygdala or sham lesions. A, Amphetamine decreased risk-taking in the sham group, with the largest effect occurring at the highest dose. B, Amphetamine decreased risk-taking in the lesion (n = 15) group to a similar extent as in shams (n = 10). Data are represented as the mean ± SEM percentage choice of the large risky reward.

Figure 6.

Effects of basolateral amygdala lesions on instrumental responding for food reward. Rats were tested under a series of fixed ratio schedules of lever pressing for food reward (FR1, FR3, FR10, FR20, and FR40), one schedule/d for 5 d. There was no difference between the lesion (n = 15) and sham (n = 10) groups on any of the individual FR schedules.

Figure 7.

Representative histology from rats that received either neurotoxic or sham lesions of the orbitofrontal cortex. A, The extent of neurotoxic lesions of the orbitofrontal cortex is depicted schematically, with the maximum lesion extent (gray) and minimum lesion extent (black) indicated in both hemispheres. B, Representative thionin-stained coronal images of the orbitofrontal cortex in a lesioned rat and a sham rat are displayed. Images were taken using a 250× objective lens.

Figure 8.

Performance in the risky decision-making task before and after orbitofrontal cortex lesions. A, Before surgery, there was no difference in choice of the large risky reward between groups that would go on to receive lesion or sham surgeries. B, After surgery, the lesion group (n = 7) showed a significant decrease in choice of the large risky reward compared with both presurgery baseline and postsurgery sham controls (n = 8). Data (mean ± SEM percentage choice of the large risky reward) are averaged over the final five sessions (both before and after surgery), at which point rats displayed stable performance.

Figure 9.

Response latencies in the risky decision-making task before and after orbitofrontal cortex lesions. A, Before surgery, all rats had significantly longer latencies to respond on the lever associated with the large risky reward compared with the lever associated with the small safe reward. B, After surgery, latencies to respond on the small reward lever were comparable between lesion and sham groups. However, the lesion group (n = 7) had significantly longer latencies than shams (n = 8) to respond on the large reward lever. Data (mean ± SEM seconds) are averaged over the final five sessions (both before and after surgery), at which point rats displayed stable performance.

Figure 10.

Effects of orbitofrontal cortex lesions on reward discrimination and instrumental responding for food reward. A, When rats were given choices between the large and small rewards in the absence of shock, both groups showed a robust preference for the large reward. There were no differences between the lesion (n = 7) and sham (n = 8) groups. Data (mean ± SEM percentage choice of the large reward) are averaged across the final five sessions, during which rats displayed stable performance. B, Rats were tested under a series of fixed ratio schedules of lever pressing for food reward (FR1, FR3, FR10, FR20, and FR40), one schedule/d for 5 d. There were no differences between the lesion and sham groups on any of the FR schedules. Data are represented as mean ± SEM.

Figure 11.

Effects of orbitofrontal cortex lesions on anxiety-like behavior. Rats were tested in the elevated plus maze during a 5 min session. A, There were no significant differences between lesion (n = 7) and sham (n = 8) groups in the number of entries made into the open, closed or center compartments. B, Similarly, there were no group differences in the amount of time spent in each of these compartments. Data for each measurement are represented as mean ± SEM.