LAUSR

HIGHLIGHTSWe investigate extinction learning with pigeons under appetitive conditions.We block NMDARs in the amygdala or the (pre)motor arcopallium during extinction.Blocking NMDARs in the amygdala impairs extinction acquisition.Blocking arcopallial NMDARs impairs consolidation of extinction memory.We show a structure‐specific dissociation of extinction encoding and consolidation. ABSTRACT Extinction learning is an essential mechanism that enables constant adaptation to ever‐changing environmental conditions. The underlying neural circuit is mostly studied with rodent models using auditory cued fear conditioning. In order to uncover the variant and the invariant neural properties of extinction learning, we adopted pigeons as an animal model in an appetitive sign‐tracking paradigm. The animals firstly learned to respond to two conditioned stimuli in two different contexts (CS‐1 in context A and CS‐2 in context B), before conditioned responses to the stimuli were extinguished in the opposite contexts (CS‐1 in context B and CS‐2 in context A). Subsequently, responding to both stimuli was tested in both contexts. Prior to extinction training, we locally injected the N‐methyl‐d‐aspartate receptor (NMDAR) antagonist 2‐Amino‐5‐phosphonovaleric acid (APV) in either the amygdala or the (pre)motor arcopallium to investigate their involvement in extinction learning. Our findings suggest that the encoding of extinction memory required the activation of amygdala, as visible by an impairment of extinction acquisition by concurrent inactivation of local NMDARs. In contrast, consolidation and subsequent retrieval of extinction memory recruited the (pre)motor arcopallium. Also, the inactivation of arcopallial NMDARs induced a general motoric slowing during extinction training. Thus, our results reveal a double dissociation between arcopallium and amygdala with respect to acquisition and consolidation of extinction, respectively. Our study therefore provides new insights on the two key components of the avian extinction network and their resemblance to the data obtained from mammals, possibly indicating a shared neural mechanism underlying extinction learning shaped by evolution.