Pavlovian conditioned diminution of the neurobehavioral response to threat

Abstract

An important function of emotion is that it motivates us to respond more effectively to threats in our environment. Accordingly, healthy emotional function depends on the ability to appropriately avoid, escape, or defend against threats we encounter. Thus, from a functional perspective, it is important to understand the emotional response to threat. However, prior work has largely focused on the emotional response in anticipation of threat, rather than the emotional response to the threat itself. The current review is focused on recent behavioral, psychophysiological, and neural findings from Pavlovian conditioning research that is centered on the expression and regulation of the emotional response to threat. The current evidence suggests that a neural network that includes the prefrontal cortex, hippocampus, and amygdala underlies learning, expression, and regulation processes that modulate emotional responses to threat. This line of research has important implications for our understanding of emotion regulation and stress resilience.

Keywords: Emotion; Learning; Pavlovian conditioning; Regulation; Threat; UCR; fMRI.

Figure 1

Illustration depicting anticipatory responses and emotional responses to threat during Pavlovian fear conditioning. A) During early conditioning trials (solid line), anticipatory responses to the warning signal are relatively small and the emotional response to the threat is relatively large. During late conditioning trials (dashed line), once the association between the warning signal and threat has formed, the warning signal elicits a relatively large anticipatory response and the predictable threat elicits a relatively small emotional response. Thus, the emotional response to threat is diminished on late compared to early conditioning trials. B) The emotional response to the unpredictable threat is similar to the response to predictable threat during early (solid line in A), but not late (dashed line in A), conditioning trials. Thus, the emotional response is larger for unpredictable (B) than for predictable (dashed line in A) threat.

Figure 2

The relationship between the anticipatory response and the response to threat (unpublished mean centered data from Knight Laboratory). As the anticipatory response increases, the response to threat decreases. The black line reflects the negative correlation that is typically observed between anticipatory responses and the emotional response to threat in Pavlovian conditioned diminution studies.

Figure 3

Regions that mediate the emotional response to threat. Arrows indicate ipsilateral connections between brain regions that regulate the emotional response to threat. The hippocampus (red) supports the development of conscious expectations of threat and projects to the dlPFC (green), vmPFC (yellow), and amygdala (blue). Anticipatory (i.e., conditioned response) dlPFC activity prior to the threat modulates the dmPFC (purple) and vmPFC response to threat (i.e., unconditioned response). Projections from the dmPFC and vmPFC regulate amygdala activity. In turn, amygdala projections to midbrain regions (e.g., the periaqueductal gray, hypothalamus, and ventral tegmental area) control the expression of the peripheral emotional response, including motor, autonomic, and hypothalamic-pituitary-adrenal axis activity.