Abstract
Understanding how learned fear can be reduced is at the heart of treatments for anxiety disorders. Tremendous progress has been made in this regard through extinction training in which the aversive outcome is omitted. However, current progress almost entirely rests on this single paradigm, resulting in a very specialized knowledgebase at the behavioural and neural level of analysis. Here, we used a dual-paradigm approach to show that different methods that lead to reduction in learned fear in rats are dissociated in the cortex. We report that the infralimbic cortex has a very specific role in fear reduction that depends on the omission of aversive events but not on overexpectation. The orbitofrontal cortex, a structure generally overlooked in fear, is critical for downregulating fear when novel predictions about upcoming aversive events are generated, such as when fear is inflated or overexpected, but less so when an expected aversive event is omitted.
Highlights
Extinction learning has captivated behavioural and neural science for more than a century
Freezing increased across days and the rate of acquisition was similar across groups as shown by a significant linear trend (tone: F(1, 45) = 69.77, p < 0.001, h2p = 0.61, 95% confidence intervals (CIs) [1.20, 1.96]; flash: F(1, 45) = 166.96, p < 0.001, h2p = 0.79, 95% CI [1.79, 2.46]), and no linear trend x training x drug interaction (tone: F(1, 45) = 0.069, p = 0.79, 95% CI [-0.84, 1.04]; flash: F(1, 45) = 0.041, p = 0.84, 95% CI [-0.75, 0.88])
Freezing increased across days and the rate of acquisition was similar across groups as shown by a significant linear trend (tone: F(1, 40) = 213.40, p < 0.001, h2p = 0.84, 95% CI [2.51, 3.31]; flash: F(1, 40) = 264.90, p < 0.001, h2p = 0.87, 95% CI [2.73, 3.50]), and no linear trend x training x drug interaction (tone: F(1, 40) = 0.15, p = 0.70, 95% CI [-0.84, 1.15]; flash: F(1, 40) = 0.007, p = 0.93, 95% CI [-0.92, 0.99])
Summary
Extinction learning has captivated behavioural and neural science for more than a century. Much progress has been made, this quest has focused on a single method for reducing learned fear: that involving outcome omission in the presence of a previously conditioned cue, while another, relevant method that drives reduction in conditioned behaviour; namely, overexpectation, remains largely unexplored. This single-paradigm approach is restrictive because at best it can oversimplify and at worst even misrepresent the function of brain areas implicated in extinction learning. We move beyond this paradigm-specific approach and embark on an investigation into how the brain learns to reduce learned fear using two behavioural designs: extinction driven by the omission of an expected aversive event (described above) and overexpectation driven by generating novel predictions that surpass the delivered aversive event (described below)
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