Fundamental contribution by the basolateral amygdala to different forms of decision making

Abstract

Impairments in decision making about risks and rewards have been observed in patients with amygdala damage. Similarly, lesions of the basolateral amygdala (BLA) in rodents disrupts cost/benefit decision making, reducing preference for larger rewards obtainable after a delay or considerable physical effort. We assessed the effects of inactivation of the BLA on risk- and effort-based decision making, using discounting tasks conducted in an operant chamber. Separate groups of rats were trained on either a risk- or effort-discounting task, consisting of four blocks of 10 free-choice trials. Selection of one lever always delivered a smaller reward (one or two pellets), whereas responding on the other delivered a larger, four pellet reward. For risk discounting, the probability of receiving the larger reward decreased across trial blocks (100-12.5%), whereas on the effort task, the larger reward was delivered after a ratio of presses that increased across blocks (2-20). Infusions of GABA agonists baclofen/muscimol into the BLA disrupted risk discounting, inducing a risk-averse pattern of choice, and increased response latencies and trial omissions, most prominently during trial blocks that provided the greatest uncertainty about the most beneficial course of action. Similar inactivations also increased effort discounting, reducing the preference for larger yet more costly rewards, even when the relative delays to reward delivery were equalized across response options. These findings point to a fundamental role for the BLA in different forms of cost/benefit decision making, facilitating an organism's ability to overcome a variety of costs (work, uncertainty, delays) to promote actions that may yield larger rewards.

Figure 1.

Task design. Cost/benefit contingencies associated with responding on either lever (left) and format of a single free-choice trial (right) of the risk (A) and effort-discounting tasks (B).

Figure 2.

Inactivation of the BLA induces risk aversion. Data are plotted as a function of the large/risky lever probability by block (x-axis). Symbols represent mean + SEM. A, Percentage choice for the large/risky lever during free-choice trials after infusions of saline or baclofen/muscimol into the BLA. Star denotes a significant (p < 0.05) main effect of treatment. B, BLA inactivations increased response latencies in the latter trial blocks. Stars denote significant (p < 0.05) differences versus saline at a specific block, and dagger denotes p < 0.05 versus all other trial blocks after BLA inactivation. C, BLA inactivations also increased trial omissions, most prominently during the latter trial blocks. Star denotes a significant (p < 0.05) main effect of treatment.

Figure 3.

Inactivation of the BLA increases effort discounting. Data are plotted as a function of the ratio on the HR lever by block (x-axis). A, Percentage of completed choices of the HR lever during free-choice trials after infusions of saline or baclofen/muscimol into the BLA. Star denotes a significant (p < 0.05) main effect of treatment. B, Response latencies were not affected by BLA inactivation.

Figure 4.

Inactivation of the BLA increases effort discounting using an equivalent delays procedure. A, Cost/benefit contingencies associated with responding on either lever on the modified effort-discounting task. B, Percentage choice of the HR lever during each trial block, averaged over the last 3 d of training on the standard effort-discounting task (diamonds) and after 5 d of training using the equivalent delays procedure (open squares). C, BLA inactivation reduced preference for the HR lever. Numbers on the abscissa denote the effort requirement on the HR lever (top) and the delay to delivery of the two pellets after a single press on the LR lever (bottom). Star denotes significant (p < 0.05) main effect of treatment. D, E, BLA inactivation increased response latencies (D) and trial omissions (E), with these effects being most prominent during the latter trial blocks. Stars denote significant (p < 0.05) differences versus saline at a specific block.

Figure 5.

BLA inactivation does not affect reward magnitude discrimination. Rats were trained to choose between two levers that delivered either a four- or one-pellet reward immediately after a single press with 100% probability. BLA inactivation did not significantly disrupt the preference for the larger four-pellet reward during free-choice trials relative to saline treatment.

Figure 6.

Histology. Schematic of coronal sections of the rat brain showing the range of acceptable location of infusions through the rostral–caudal extent of the BLA for all rats trained on the risk (triangles) or effort (circle) discounting tasks. Numbers beside each plate correspond to millimeters from bregma.