Opposing effects of rewarding and aversive stimuli on D1 and D2 types of dopamine-sensitive neurons in the central amygdala

Abstract

Dopamine-sensitive neurons are organized in two classes of cells, expressing D1- or D2- types of dopamine receptors, and are often mediating opposing aspects of reward-oriented behaviors. Here, we focused on dopamine-sensitive neurons in the central amygdala - a brain structure critically involved in processing emotion-related stimuli. We discovered that both dopamine receptor types are present in the central medial nucleus, while the lateral part is populated predominantly with DRD2 cells. Exposing mice to rewarding and aversive stimuli we studied DRD1 and DRD2 cells activity using in vivo two-photon calcium imaging in the CeM. We showed that cocaine and sugar predominantly increase the activity of DRD1(+) neurons and decrease DRD2(+) cells. Repeated exposure to cocaine, however, had the opposite effect on spontaneous excitatory synaptic transmission in the CeM than exposure to sugar. Quinine, an aversive stimulus, primarily engaged DRD2(+) neurons, activating predominantly those cells that were previously inhibited by sugar exposure. Our results show that though DRD1 and DRD2 populations are differentially engaged and regulated by appetitive/aversive stimuli, both participate in sugar, cocaine, and quinine processing.