Frustrative nonreward, sucrose consumption, and the basal ganglia: Role of chemogenetic activation of projections from the nucleus accumbens to the globus pallidus internus, globus pallidus externus, and ventral pallidum

Mammals experience negative emotions after the unexpected reduction in reward magnitude-called frustrative nonreward (FNR). The neurobiological mechanisms activated in response to unexpected reward downshift could shed light on loss-induced anxiety, conflict, mood, and physical pain. Experiment 1 examined the role of three basal ganglia (BG) pathways in the adjustment to unexpected sucrose downshifts. A double-infection chemogenetic procedure was used to activate neurons in the nucleus accumbens (NAc) that project to the globus pallidus externus (GPe), globus pallidus internus (GPi), or ventral pallidum (VP) during a 32-to-2% sucrose downshift. Activation of the NAc-to-GPe pathway had no observable effects on licking during reward downshift, whereas activation of either the NAc-to-GPi or NAc-to-VP pathways caused significant consummatory suppression. Chemogenetic activation of the NAc-to-GPi and NAc-to-VP pathways also yielded increased consummatory suppression in animals exposed to either 2% sucrose (Experiment 2) or 32% sucrose (Experiment 3) in the absence of a sucrose downshift. These effects were accompanied by no evidence of motor dysfunction in the open field and a nonsignificant trend toward a decrease in sucrose palatability, particularly with a choice between 2% sucrose and water. However, preliminary observations show that licking suppression after CNO injections also enhanced activity in the conditioning box during access to 32% sucrose and relative to vehicle injections. Thus, these BG pathways regulate consummatory behavior in different ways, but whether BG dysfunction influences the behavioral response to unexpected reward downshifts remains to be established.