A critical contribution of a sparse neuronal ensemble in the amygdala central nucleus to extinction

Abstract

Adaptive behaviour critically depends on the delicate and dynamic balance between acquisition and extinction memories. Disruption of this balance, particularly when the extinction memory loses control over behaviour, is the root of treatment failure of maladaptive behaviours such as substance abuse or anxiety disorders. Understanding this balance requires a better understanding of the underlying neurobiology and its contribution to behavioural regulation. Here, we used Daun02 in Fos-lacZ transgenic rats to delete extinction-recruited neuronal ensembles in BLA and CN and examine their contribution to behaviour in an appetitive Pavlovian task. Deletion of extinction-activated ensembles in CN but not BLA impaired the retrieval of extinction and increased activity in the BLA. The disruptive effect of deleting these CN ensembles was enduring as it hindered further extinction learning, and promoted greater levels of behavioural restoration across opposing levels of the response scale seen in spontaneous recovery and reinstatement. Our data indicate that the initial extinction-recruited CN ensemble is critical to the acquisition-extinction balance, and that greater behavioural restoration does not mean weaker extinction contribution. These findings provide a novel avenue for thinking about the neural mechanisms of extinction and in developing treatments for cue-triggered appetitive behaviours.