Faculty Bibliography

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.

Novel events produce characteristic orienting responses (ORs), which typically habituate rapidly with repeated stimulus presentation. However, they may re-emerge if those stimuli become predictors of biologically significant events. This acquisition of conditioned ORs may reflect a broader range of enhancements in top-down attentional processing of cues that predict important consequences. Previous research from this laboratory showed that a neural circuit that includes the amygdala central nucleus (CeA), substantia nigra pars compacta (SNc) and dorsolateral striatum (DLS) is essential for the learning and expression of one example of conditioned orienting, the rearing of rats to visual stimuli paired with food. Other studies showed that the CeA is critical to the acquisition of these conditioned ORs, but not their expression, and that normal DLS function is required for the expression of previously acquired conditioned ORs, but not for learning itself. The experiments reported here considered the roles of the SNc in conditioned orienting by examining the effects of transient inactivation of the SNc during the acquisition of new associations and during the expression of previous learning. SNc function was critical to both the acquisition and expression of conditioned ORs but not to the display of unconditioned ORs or the learning and expression of conditioned responses directed to the food source. Together with our previous findings, these results suggest that the SNc is trained by the CeA during learning and maintains acquired information so that it may modulate DLS sensory-motor function at the time of action.