The Role of the Primate Amygdala in Conditioned Reinforcement

Abstract

Conditioned reinforcement refers to the capacity of a conditioned stimulus to support instrumental behavior by acquiring affective properties of the primary reinforcer with which it is associated. Conditioned reinforcers maintain behavior over protracted periods of time in the absence of, and potentially in conflict with, primary reinforcers and as such may play a fundamental role in complex social behavior. A relatively large body of evidence supports the view that the amygdala (and in particular the basolateral area) contributes to conditioned reinforcement by maintaining a representation of the affective value of conditioned stimuli. However, a recent study in primates (Malkova et al., 1997), using a second-order visual discrimination task, suggests that the amygdala is not critical for the conditioned reinforcement process. In the present study, excitotoxic lesions of the amygdala in a new world primate, the common marmoset, resulted in a progressive impairment in responding under a second-order schedule of food reinforcement. In addition, the responding of amygdala-lesioned animals was insensitive to the omission of the conditioned reinforcer, unlike that of control animals, for which responding was markedly reduced. In contrast, lesioned animals were unimpaired when responding on a progression of fixed-ratio schedules of primary reinforcement. These data confirm that the amygdala is critical for the conditioned reinforcement process in primates, and taken together with other recent work in monkeys, these results suggest that the contribution of the amygdala is to provide the affective value of specific reinforcers as accessed by associated conditioned stimuli.

Lesions of Orbitofrontal Cortex Impair Rats' Differential Outcome Expectancy Learning But Not Conditioned Stimulus-Potentiated Feeding

“…Furthermore, these authors suggested that this learned motivational function of the OFC depends on its interaction with the BLA, as we discussed earlier in the case of learned outcome expectancies. Consistent with this claim, although a CS paired with food typically acquires the ability to serve as a conditioned reinforcer (Fantino, 1977;Rescorla, 1980), that ability is impaired in animals with lesions of either the BLA (Cador et al, 1989;Burns et al, 1993;Hatfield et al, 1996;Parkinson et al, 2001) or the OFC (Pears et al, 2003). It seemed reasonable to anticipate that another BLA-dependent motivational function acquired by a CS paired with food, the potentiation of feeding in satiation , would also critically involve the OFC; however, the results of experiment 1 indicate that BLA-OFC connectivity is not critical to this function.…”

GABAA-Mediated Inhibition of Basolateral Amygdala Blocks Reward Devaluation in Macaques

“…These associations include those required for fear conditioning as well as those involved in processing reward and linking sensory stimuli with positive reinforcement (for review, see Baxter and Murray, 2002). By registering the current value of positive reinforcement, the amygdala may guide goal-oriented behavioral action and permit shifts in behavior in response to outcomes (Hatfield et al, 1996;Malkova et al, 1997;Schoenbaum et al, 1998Schoenbaum et al, , 1999Schoenbaum et al, , 2003Blundell et al, 2001Blundell et al, , 2003Parkinson et al, 2001;Balleine et al, 2003). Under conditions in which animals are required to adjust behavior based on changes in the value of the reinforcer, the integrity of the amygdala has been found to be critical.…”

Neuronal Signals in the Monkey Basolateral Amygdala during Reward Schedules

“…For example, functional neuroimaging studies in humans show that the amygdala is activated during recognition of fearful and happy facial expressions (Morris et al, 2002;Hare et al, 2005). The amygdala also appears to be involved in evaluating the reward value of a stimulus (Malkova et al, 1997;Parkinson et al, 2001). All of these findings are consistent with the view that the amygdala is important for assessing the affective (or emotional) valence of a stimulus and/or production of a specific affective state (Everitt et al, 2003;Phillips et al, 2003).…”