Trace Conditioning in Drosophila Induces Associative Plasticity in Mushroom Body Kenyon Cells and Dopaminergic Neurons

Abstract

Dopaminergic neurons (DANs) signal punishment and reward during associative learning. In mammals, DANs show associative plasticity that correlates with the discrepancy between predicted and actual reinforcement (prediction error) during classical conditioning. Also in insects, such as Drosophila, DANs show associative plasticity that is, however, less understood. Here, we study associative plasticity in DANs and their synaptic partners, the Kenyon cells (KCs) in the mushroom bodies (MBs), while training Drosophila to associate an odorant with a temporally separated electric shock (trace conditioning). In most MB compartments DANs strengthened their responses to the conditioned odorant relative to untrained animals. This response plasticity preserved the initial degree of similarity between the odorant- and the shock-induced spatial response patterns, which decreased in untrained animals. Contrary to DANs, KCs (α'/β'-type) decreased their responses to the conditioned odorant relative to untrained animals. We found no evidence for prediction error coding by DANs during conditioning. Rather, our data supports the hypothesis that DAN plasticity encodes conditioning-induced changes in the odorant's predictive power.

Learning with reward prediction errors in a model of the Drosophila mushroom body

“…Below, we specify which model supports each prediction. (36) reported such decaying responses in DANs in the γ-and β -lobes during paired CS+ and US stimulation. However, they reported similar decaying responses when the CS+ and US were unpaired (separated by 90 seconds) that were not significantly different from the paired condition.…”

“…Ultimately, the evidence for either effect is insufficient. Moreover, Dylla et al (36) observed increases in DAN responses to the CS+ during training. This is consistent with the temporal difference learning algorithm (37; 38), which is an extension of the Rescorla-Wagner rule.…”

Multilevel feedback architecture for adaptive regulation of learning in the insect brain

“…7e). Such responses have been observed in modulatory neurons of species across the animal kingdom 12,23,32 , including adult and larval Drosophila 43,44,144 . They are consistent with a computa-tion of the valence of the US that is predicted by the CS+ (i.e.…”

Recurrent loops: Incorporating prediction error and semantic/episodic theories into Drosophila associative memory models

“…Flies exhibit various olfactory associative behaviors that cannot be explained by the models presented here. For example, similar to other organisms, flies can form associations between stimuli that are not presented simultaneously, but instead presented in a predictable temporal order, a type of memory known as trace memory . Thus, flies can form associations between a CS and a US when the US is presented after termination of the CS.…”

“…For example, similar to other organisms, flies can form associations between stimuli that are not presented simultaneously, but instead presented in a predictable temporal order, a type of memory known as trace memory. [68][69][70] Thus, flies can form associations between a CS and a US when the US is presented after termination of the CS. This type of memory also requires the MBs, suggesting that the MBs maintain a CS memory trace in the absence of a US.…”