Contrasting roles of basolateral amygdala and orbitofrontal cortex in impulsive choice

Abstract

The orbitofrontal cortex (OFC) and basolateral nucleus of the amygdala (BLA) share many reciprocal connections, and a functional interaction between these regions is important in controlling goal-directed behavior. However, their relative roles have proved hard to dissociate. Although injury to these brain regions can cause similar effects, it has been suggested that the resulting impairments arise through damage to different, yet converging, cognitive processes. Patients with OFC or amygdala lesions exhibit maladaptive decision making and aberrant social behavior often described as impulsive. Impulsive choice may be measured in both humans and rodents by evaluating intolerance to delay of reinforcement. Rats with excitotoxic lesions of the BLA and OFC were tested on such a delay-discounting procedure. Although lesions of the BLA increased choice of the small immediate reward, indicating greater impulsivity, OFC lesions had the opposite effect, increasing preference for the larger but delayed reward. The fact that the delay did not devalue the large reward to such an extent in OFC-lesioned animals supports the suggestion that the OFC is involved in updating the incentive value of outcomes in response to devaluation. In contrast, the BLA-lesioned animals markedly decreased their preference for the large reward when it was delayed, potentially because of an inability to maintain a representation of the reward in its absence. This is the first time that lesions to these two structures have produced opposite behavioral effects, indicating their distinct contributions to cognition.

Figure 1.

A, B, Basic outline of the delay-discounting task in terms of the sequence of events in a trial (A) and the timeline of the experiment (B).

Figure 2.

A–D, Photomicrographs depicting a typical OFC lesion (B) and BLA lesion (D) compared with appropriate sham control tissue (A and C, respectively). MO, Medial orbital cortex; VO, ventral orbital cortex; LO, lateral orbital cortex; AI, agranular insular cortex; CeN, central amygdaloid nucleus.

Figure 3.

Effect of lesions to the OFC and BLA on performance of a delay-to-gratification task compared with sham-operated controls. Data shown are mean number of responses and SEM taken from seven consecutive postoperative sessions.