Review
Cognitive-emotional interactions
The amygdala, reward and emotion

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Recent research provides new insights into amygdala contributions to positive emotion and reward. Studies of neuronal activity in the monkey amygdala and of autonomic responses mediated by the monkey amygdala show that, contrary to a widely held view, the amygdala is just as important for processing positive reward and reinforcement as it is for negative. In addition, neuropsychological studies reveal that the amygdala is essential for only a fraction of what might be considered ‘stimulus-reward processing’, and that the neural substrates for emotion and reward are partially nonoverlapping. Finally, evidence suggests that two systems within the amygdala, operating in parallel, enable reward-predicting cues to influence behavior; one mediates a general, arousing effect of reward and the other links the sensory properties of reward to emotion.

Introduction

The amygdala is a unique part of the telencephalon. In primates, it appears almond shaped and lies in the anterior temporal lobe, toward its medial side (Figure 1a, b). Although sometimes treated as a single ‘thing’ [1], the amygdala contains an enormous diversity of nuclei and cell types (Figure 1a, c). It receives projections from most cortical fields 2, 3, 4, 5, 6, 7, and usually returns them 8, 9, 10, 11. These anatomical facts, alone, illustrate the pivotal position of the amygdala in the telencephalon.

According to current thinking, the amygdala contributes to emotion, reward, motivation, learning, memory and attention. Yet the relationship among these cognitive processes, and the specific contribution of the amygdala to them, remains one of the central challenges in cognitive neuroscience. To complicate matters, ‘reward’ is not a unitary construct; rewards have sensory, affective and motivational properties, each of which is represented in the brain 12, 13, 14. As an operational definition, ‘reward’ and ‘reinforcement’ are used interchangeably here to refer to something that an animal will work to obtain (if positive) or avoid (if negative). Reinforcement received after performance of an action also functions to increase the probability that the same action will be repeated, although this phenomenon will not be discussed further here. In addition, however, rewards might influence behavior through Pavlovian mechanisms that operate independently of actions. Because the content of emotion is inaccessible in nonhuman subjects, and is outside the scope of this article (but see Barrett et al. [15]), the term ‘emotion’ is used here for reactions to stimuli, including autonomic and skeletal motor ones. Finally, ‘valence’ is used to refer to the direction of value assignment (either positive or negative) as opposed to its absolute value or intensity, and ‘affect’ to refer collectively to the neural representations and processes related to emotion.

Three main themes are developed here. First, contrary to a widespread view, the amygdala has a major role in positive affect, not exclusively – or even mainly – in negative affect. Second, contrary to an influential model, recent evidence points to a distinction between emotion and reward and contradicts previous conclusions about the role of the amygdala in reward processing. Third, contrary to the tendency to consider the amygdala as a single ‘thing’, different parts of the amygdala mediate specific and general effects of reward on behavior.

Section snippets

Amygdala function in positive affect

The idea that the amygdala functions primarily in negative affect remains firmly entrenched, as evidenced by theories treating the amygdala as a ‘protection device’ that prevents animals from engaging in potentially harmful behaviors [16] or as a ‘fear module’ [17]. In part, this impression results from the dominance of fear conditioning as a model of emotional learning 18, 19. Neuroimaging studies, especially early ones, also viewed the amygdala as processing primarily negative emotions [20].

Amygdala function in emotion versus reward

In an influential two-dimensional model of emotion, developed by Rolls [35], emotions are seen as by-products of positive and negative reinforcement. One dimension comes from administration of negative reinforcement to administration of positive reinforcement, which corresponds to emotions ranging from fear to pleasure, respectively. The second dimension comes from termination or omission of positive or negative reinforcers, with emotions ranging from rage to relief, respectively. This model

Amygdala function in specific and general affect

The discussion to this point has focused on two dichotomies: one involving positive versus negative affect, the other involving reward processing versus emotional reactions. This section deals with a third dichotomy: specific versus general affect.

Recent research in rats suggests contrasting roles for the BLA and the CeA in affective processing. Several studies have demonstrated a role for CeA in positive affect. Its role in Pavlovian approach behavior, for example, has been described earlier.

Amygdala function: passions and prejudices

The function of the amygdala is more general than often thought: it contributes to both positive and negative affect, not just – or even mainly – to negative affect. Its function is also more specific than some current theories suggest: it makes an essential contribution to emotional responses, such as reactions to a fake snake or to the sight of food, yet has little or no role in the reward processing that underlies tasks such as object-reversal learning and win-stay, lose-shift. These

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