Roles of dopamine neurons in mediating the prediction error in aversive learning in insects

Kanta Terao,Makoto Mizunami

doi:10.1038/s41598-017-14473-y

Abstract

In associative learning in mammals, it is widely accepted that the discrepancy, or error, between actual and predicted reward determines whether learning occurs. The prediction error theory has been proposed to account for the finding of a blocking phenomenon, in which pairing of a stimulus X with an unconditioned stimulus (US) could block subsequent association of a second stimulus Y to the US when the two stimuli were paired in compound with the same US. Evidence for this theory, however, has been imperfect since blocking can also be accounted for by competitive theories. We recently reported blocking in classical conditioning of an odor with water reward in crickets. We also reported an “auto-blocking” phenomenon in appetitive learning, which supported the prediction error theory and rejected alternative theories. The presence of auto-blocking also suggested that octopamine neurons mediate reward prediction error signals. Here we show that blocking and auto-blocking occur in aversive learning to associate an odor with salt water (US) in crickets, and our results suggest that dopamine neurons mediate aversive prediction error signals. We conclude that the prediction error theory is applicable to both appetitive learning and aversive learning in insects.

Highlights

Associative learning allows animals to adapt to various environments by acquiring knowledge on events in their environments
We used odor-pattern compound conditioning (OP+ conditioning), in which a compound stimulus consisting of an odor (O) and a visual pattern (P) is paired with a 20% NaCl solution (+), and we investigated whether OP+ training leads to learning of the odor or the visual pattern (Fig. 1 and Table 1)
At first, that a blocking phenomenon occurs in aversive learning in crickets, i.e., no learning of Y occurred by XY+ training when the training was preceded by X+ training with X and Y being either visual or olfactory stimulus

Summary

Introduction

Associative learning allows animals to adapt to various environments by acquiring knowledge on events in their environments. We obtained evidence that octopamine (OA) neurons play critical roles in appetitive learning in crickets[12,13,14,15,16,17,18,19], and we demonstrated that when a stimulus X was paired with water (appetitive US) under the condition of administration of an OA receptor antagonist, in which no learning of X occurs, subsequent learning of X was blocked in training to associate the stimulus X with the US given after recovery from the effect of the antagonist[11] This “auto-blocking” can be accounted for by the prediction error theory since if blockade of OA-ergic transmission impairs learning but not formation of the prediction of the US by stimulus X, no learning of stimulus X should occur in subsequent training. This “auto-blocking” phenomenon cannot be accounted for by any of the competitive theories www.nature.com/scientificreports/

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