Contrasting Role of Octopamine in Appetitive and Aversive Learning in the Crab Chasmagnathus

Laura Kaczer,Héctor Maldonado,Björn Brembs

doi:10.1371/journal.pone.0006223

Abstract

BackgroundBiogenic amines are implicated in reinforcing associative learning. Octopamine (OA) is considered the invertebrate counterpart of noradrenaline and several studies in insects converge on the idea that OA mediates the reward in appetitive conditioning. However, it is possible to assume that OA could have a different role in an aversive conditioning.Methodology/Principal FindingsHere we pharmacologically studied the participation of OA in two learning processes in the crab Chasmagnathus granulatus, one appetitive and one aversive. It is shown that the aversive memory is impaired by an OA injection applied immediately or 30 minutes after the last training trial. By contrast, the appetitive memory is blocked by OA antagonists epinastine and mianserine, but enhanced by OA when injected together with the supply of a minimum amount of reinforcement. Finally, double-learning experiments in which crabs are given the aversive and the appetitive learning either successively or simultaneously allow us to study the interaction between both types of learning and analyze the presumed action of OA. We found that the appetitive training offered immediately, but not one hour, after an aversive training has an amnesic effect on the aversive memory, mimicking the effect and the kinetic of an OA injection.Conclusions/SignificanceOur results demonstrate that the role of OA is divergent in two memory processes of opposite signs: on the one hand it would mediate the reinforcement in appetitive learning, and on the other hand it has a deleterious effect over aversive memory consolidation.

Highlights

Conclusions/Significance: Our results demonstrate that the role of OA is divergent in two memory processes of opposite signs: on the one hand it would mediate the reinforcement in appetitive learning, and on the other hand it has a deleterious effect over aversive memory consolidation
The role of octopamine (OA) in learning processes has been extensively studied in insects, showing that this amine, often considered a functional homologue of vertebrate’s noradrenaline [1,2,3], mediates the reinforcement in appetitive learning
In fruit-flies, appetitive learning with sugar reward is blocked in transgenic individuals defective in OA synthesis [6]; and in crickets, pharmacological blockade of OA receptors resulted in a complete impairment of appetitive visual learning [7] and appetitive olfactory learning [8] both with water reward

Summary

Introduction

The role of octopamine (OA) in learning processes has been extensively studied in insects, showing that this amine, often considered a functional homologue of vertebrate’s noradrenaline [1,2,3], mediates the reinforcement in appetitive learning. In fruit-flies, appetitive learning with sugar reward is blocked in transgenic individuals defective in OA synthesis [6]; and in crickets, pharmacological blockade of OA receptors resulted in a complete impairment of appetitive visual learning [7] and appetitive olfactory learning [8] both with water reward. All in all, these studies agreed with the idea that OA would act as a positive token, signalling a positive reward in an appetitive conditioning. It is possible to assume that OA could have a different role in an aversive conditioning

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