Dissociable effects of disconnecting amygdala central nucleus from the ventral tegmental area or substantia nigra on learned orienting and incentive motivation

Recent evidence suggests that the amygdala central nucleus (CeA) and midbrain-striatal dopamine systems are critically involved in the alteration of attentional and emotional processing of initially neutral stimuli by associative learning. In rats, the acquisition of learned orienting responses (ORs) to visual cues paired with food is impaired by lesions of the CeA, and by lesions that disconnect CeA from the dorsolateral striatum (DLS), a region traditionally implicated in elevated responsiveness to sensory stimuli. Similarly, the acquisition of emotional significance to cues paired with food also depends on the function of CeA and of the ventral striatal nucleus accumbens (ACB), a region often considered crucial to acquired reward and motivation. For example, the ability of a cue previously paired with food to increase the rate of food-reinforced instrumental responding (Pavlovian-instrumental transfer, PIT) is eliminated by lesions of the CeA or the accumbens core. In this experiment, we found that lesions that functionally disconnected CeA from the substantia nigra pars compacta (SNc) impaired the acquisition of conditioned orienting to auditory cues paired with food, but had no effect on their ability to enhance instrumental responding, relative to the effects of unilateral lesions of that region. By contrast, lesions that disconnected CeA from the ventral tegmental area (VTA) had no effect on the acquisition of conditioned orienting, but facilitated Pavlovian-instrumental transfer relative to unilateral midbrain lesions, rescuing that function to sham–lesion control levels. Otherwise, unilateral lesions of either midbrain region impaired transfer. Implications of these results for circuit models of amygdalo–striatal interactions in associative learning are discussed.