Wanting what hurts: D1 dopamine neuronal stimulation in CeA is sufficient to induce maladaptive attraction

Maladaptive desires, such as addictions, can arise and persist even when their outcome is not enjoyed. A laboratory prototype of maladaptive desire is ‘wanting what hurts’. This has been produced in rats by pairing optogenetic stimulations of neurons in central nucleus of amygdala (CeA) with voluntary encounters of an electrified shock rod. However, it remains unknown which particular CeA neuronal subtypes can generate maladaptive attraction. Here we used Cre targeted optogenetic stimulation to assess relative contributions of CeA neuronal subtypes that express D1 dopamine receptors, D2 dopamine receptors, or CRF as neurotransmitter. We report that selective stimulation of D1-expressing CeA neurons is sufficient to induce shock rod attraction, similar to that produced by hSyn-targeted stimulation of general CeA neuronal populations. Both caused similar levels of self-administered shocks. CeA D1 rats and CeA hSyn rats were also motivated to overcome a barrier to reach the shock rod, and to seek out Pavlovian cues associated with shocks from the shock rod. These features, plus mesolimbic Fos activation, indicated that maladaptive attraction was mediated by incentive motivation mechanisms usually reserved for rewards. Our results reveal a special role for D1-expressing CeA neurons in producing ‘wanting what hurts’ as a prototype of addictive-like motivation.