amygdala

Role in innate and learned emotional behaviour

Pheromones and innately appetitive and aversive stimuli, including certain odours, tastes, or sexual imagery, can produce physiological and behavioral expressions of emotional state. For olfactory stimuli, the cortico-medial amygdala is known to mediate innate emotional behaviour. For other innately reinforcing stimuli, including some drugs of abuse, circuitry within the basolateral complex likely also contributes to emotional responses.

Emotional learning most commonly has been studied in both animal models and humans, using Pavlovian conditioning, in which an otherwise neutrally conditioned stimulus is paired with an innately aversive unconditioned stimulus. This type of paradigm, often referred to as fear conditioning, can result in robust learning, owing to the convergence of sensory information about the conditioned stimulus and the unconditioned stimulus. Neuromodulatory input may also contribute to this learning. As an animal learns, the responses of amygdala neurons to conditioned stimuli change, reflecting the learning process. Furthermore, the activation of neurons in the basolateral amygdala can induce learning, suggesting that those neurons play a causal role in emotional learning. After learning, input from the basolateral complex to the central nucleus of the amygdala leads to the orchestration of a range of physiological and behavioral responses that are correlated with emotional states. Measures of fear conditioning include the cessation of movement (“freezing”), a defensive behaviour, and increased skin conductance responses or increased blood pressure (autonomic measures that reflect arousal level). Lesions of the amygdala impair the acquisition and expression of this learning.

Although the study of the amygdala has been most extensively pursued by means of aversive stimuli, there is substantial evidence that the amygdala is also involved in the processing of rewarding stimuli and in appetitive learning. Within the amygdala neural responses to conditioned stimuli change during appetitive learning, and many amygdala neurons respond to different rewarding stimuli. The activation of amygdala neurons that respond to a rewarding stimulus can induce both Pavlovian and instrumental learning (learning in which behaviour is influenced by consequences). A pathway from the amygdala to the ventral striatum, which has been implicated in reward processing in addiction, mediates learned approach behaviours (movements toward objects or other individuals). However, amygdalar lesions often do not impair appetitive learning, indicating that such learning is likely also supported by parallel neural pathways that do not involve the amygdala.

Regulation of emotion

Emotional responses to sensory stimuli not only arise through innate mechanisms and through learning but also can be altered by extinction and cognitive control mechanisms. Both extinction and cognitive control involve interactions between the prefrontal cortex and the amygdala. Extinction, which itself is a learning process, is induced by the repeated presentation of a conditioned stimulus in the absence of a previously associated unconditioned stimulus, resulting in the elimination of a previously elicited response. Projections from the prefrontal cortex to the amygdala mediate extinction, with complex circuitry involving the central nucleus, the basolateral complex, and the intercalated masses playing a role in the modification of responses to previously conditioned stimuli.

The cognitive control of emotion is an important process to understand, given its critical role in normal adaptive emotional behaviour. Human studies using functional magnetic resonance imaging have implicated prefrontal-amygdala interactions in these processes, though the precise mechanisms remain poorly understood, in part owing to the difficulty in studying those processes in animal models.

The amygdala, cognition, and social behaviour

Emotions influence cognitive processes such as attention, memory formation, and decision making, and they play a prominent role in social behaviour. A large body of literature supports a role for the amygdala in those functions, presumably by virtue of amygdalar projections to the prefrontal and sensory cortices, to the hippocampus and rhinal cortices, and to subcortical neuromodulatory systems. For example, patients with isolated lesions of the amygdala resulting from Urbach-Wiethe disease (a rare genetic disorder) can exhibit a deficit in identifying fearful facial expressions. That deficit appears to be due to difficulties in directing attention to the eyes of others, which is important for discerning fear. Consistent with that observation, amygdala neural activity can reflect the emotional significance and location of visual stimuli. Substantial work also implicates a role for the basolateral amygdala in modulating the formation of memories in relation to emotional events. In addition, human neuroimaging studies suggest a role for the amygdala in mediating the so-called framing effect during economic choices, which is thought to reflect the effect of positive or negative emotion on decision making.