Interactions between orbital prefrontal cortex and amygdala: advanced cognition, learned responses and instinctive behaviors

Abstract

Recent research indicates that the orbital prefrontal cortex (PFo) represents stimulus valuations and that the amygdala updates these valuations. An exploration of how PFo and the amygdala interact could improve the understanding of both. PFo and the amygdala function cooperatively when monkeys choose objects associated with recently revalued foods. In other tasks, they function in opposition. PFo uses positive feedback to promote learning in object-reward reversal tasks, and PFo also promotes extinction learning. Amygdala function interferes with both kinds of learning. The amygdala underlies fearful responses to a rubber snake from the first exposure on, but PFo is necessary only after the initial exposure. The amygdala mediates an arousal response in anticipation of rewards, whereas PFo sometimes suppresses such arousal. A role for PFo in advanced cognition, for the amygdala in instinctive behavior, and for cortex-subcortex interactions in prioritizing behaviors provides one account for these findings.

Figure 1

Reinforcer devaluation. (a) Macaque monkeys chose between two objects, each associated with a different kind of food. Prior to the choice tests, one of the two foods had been devalued via selective satiation. Plot summarizes data from three different studies to show results from intact, control monkeys (pooled across studies) and monkeys with bilateral lesions of the amygdala [6], bilateral lesions of orbital prefrontal cortex (PFo), and crossed disconnection (illustrated in the inset) of the amygdala (A) from PFo (PFo × A). Each operated group differs significantly from controls. Error bars: SEM. (b) Results [7•,8•] from control monkeys and monkeys with bilateral lesions of the dorsolateral prefrontal cortex (area 46, PFdl), ventral prefrontal cortex (area 12, PFv), and PFo. *, significantly different from controls.

Figure 2

Amygdala and PFo contributions to three behavioral tests in macaque monkeys. (a) Serial object-reversal learning [10••]. In this task, monkeys chose between two objects, and only one choice produced a food reward. The choice that did so changed periodically. Across a series of such reversals, monkeys with bilateral lesions of orbital prefrontal cortex (PFo) benefited less than controls after two, three or four correct (C) choices following an error (E) [EC(2)+1, EC(3)+1, and EC(4)+1 trial types, respectively]. Monkeys with bilateral amygdala (Amyg) lesions benefited more than controls when an error trial was followed by a single correct choice (EC+1 trial type). *, significantly different from controls. (b) Extinction. Monkeys first learned to displace a single object to obtain a food reward hidden underneath. After five consecutive days of consistently displacing the object to obtain food reward (acquisition, acq), object displacement failed to produce food over the next five days [12]. (c) Snake test. Food-retrieval rates when monkeys had to reach over a rubber snake to retrieve food [13]. Amygdala lesion group differed significantly from controls on all five sessions, whereas PFo group differed from controls on sessions 3–5 only. The fastest retrieval rates matched closely the times for reaching over neutral objects. Error bars: SEM.

Figure 3

Pavlovian conditioning in marmoset monkeys. (a) Over several trials, marmosets saw a highly valued food for 20 s before being allowed to consume it. In intact monkeys, systolic blood pressure (BP) increased during the 20-s anticipatory phase; the amygdala lesion group displayed significantly lower BP relative to controls [15]. The Measure: millimeters of mercury (Hg). (b) First, marmosets learned that a tone (the conditioned stimulus, CS) indicated the availability of food (the unconditioned stimulus, US) during CS presentation. On a subsequent probe trial, the tone stopped (CS off) and the predicted food failed to appear (US omission). Points to left show BP during tone presentation; the series of points to the right show BP as a function of time after CS offset on the probe trial [16••]. Error bars: SEM.

Figure 4

Scheme of interactions among cortical (top row) and subcortical (middle row) structures. According to this scheme, the granular prefrontal cortex prioritizes learned strategies, rules and other aspects of advanced cognition; the agranular frontal cortex prioritizes behaviors based on learned associations among stimuli (S), responses (R), and outcomes (O); and the hippocampal cortex and amygdala prioritize innate behaviors. The granular prefrontal cortex also implements advanced cognition by suppressing conditioned behaviors when warranted, and both the granular and agranular parts of frontal cortex suppress innate behaviors when warranted. Cortical-field abbreviations from left to right: PFo, PFdl and PFv, orbital, dorsolateral and ventral prefrontal cortex, respectively; IL, infralimbic cortex; PL, prelimbic cortex; AC, anterior cingulate cortex; OFa, agranular orbitofrontal cortex; Ia, agranular insular cortex.