Temporally limited role of substantia nigra-central amygdala connections in surprise-induced enhancement of learning.

Prediction error plays an important role in modern associative learning theories. For example, the omission of an expected event (surprise) can enhance attention to cues that accompany those omissions, such that subsequent new learning about those cues is more rapid. Many studies from our laboratories have demonstrated that circuitry that includes the amygdala central nucleus (CeA), the cholinergic neurons in the substantia innominata/nucleus basalis region and their innervation of the posterior parietal cortex is critical for this surprise-induced enhancement of attention in learning. We recently showed that midbrain dopamine neurons, known to code prediction error, are also important for surprise-induced enhancement of learning through their interaction with CeA. The present study examined whether in rats the communication between the substantia nigra pars compacta (SNc) and CeA is critical only at the time of surprise, for example to detect prediction error information, or is also needed to maintain and later express that information as enhanced learning. All animals received unilateral CeA lesions and unilateral cannula implants targeting the SNc located contralateral to the lesioned CeA. As the SNc-CeA connections are mainly ipsilateral, inactivating SNc contralateral to the lesioned CeA provided transient blockage of SNc and CeA communication. The results show that SNc-CeA communication is critical for processing prediction error information at the time of surprise, but neither SNc nor SNc-CeA communication is necessary to express that information as enhanced learning later.