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

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.

Aversive conditioning in honey bees (Apis mellifera anatolica): a comparison of drones and workers

“…In addition, the results of escape conditioning are similar to those found with food rewards (see Mackintosh, 1974). Here, an aversive event is presented when the response occurs (Kaczer and Maldonado, 2009), and is ideal for researchers looking for a protocol that produces the opposite effect of escape training.…”

Parallel memory traces are built after an experience containing aversive and appetitive components in the crab Neohelice

“…This result was possible because the behaviors that evidence appetitive and aversive memories are not mutually exclusive. The behavioral output that makes evident contextual appetitive memory is an increase in the exploratory activity upon placement of the animal in the training context, whereas contextual aversive memory is revealed by a decrease in escape response elicited by the danger stimulus in the same context (6,18). It is important to remark that although the aversive memory requires stimulation with the danger stimulus to be disclosed, the reactivation of it already occurs during reexposure to the training context at the same time that the appetitive memory is being expressed, as it is proved by the reconsolidation experiments.…”

“…In light of the present result, we interpret that dopamine injection emulates part of the effects that aversive training cause on appetitive memory. In regard to appetitive learning, octopamine is needed to elicit the formation of appetitive memory in crabs, honey bees, and crickets (1,3,6). Interestingly, injection of octopamine coincident with aversive training impairs formation of long-term aversive memory in crabs and honey bees (6,8).…”

“…Invertebrates are convenient models to study the interaction between appetitive and aversive memory processes because neurochemical pathways and circuits involved in both types of memory have begun to be elucidated (1)(2)(3)(4)(5). The hypothesis that appetitive and aversive information interact during memory processes gets support from pharmacological studies in crabs (6,7) and bees (8,9), which show that the neurotransmitter necessary for appetitive memory formation does, in turn, impair aversive memory, whereas the transmitter necessary for aversive memory impairs appetitive memory. In addition, studies in Drosophila, in which memory mechanisms can be dissected at the neuron level, provide evidence that the interaction between appetitive and aversive information occurs from the circuits that encode reward and punishment to circuits that regulate memory expression (10)(11)(12)(13)(14).…”

“…Here, we have addressed this question by using the crab Neohelice considering advantages that it offers for this study: It has two well-described appetitive and aversive memory paradigms (6,18), both are contextual associative memories that use the same context as conditioned stimulus, and finally, appetitive and aversive memories become evident by two nonmutually exclusive behaviors. This last attribute allows that, if two different memories associated to the same context are formed, then they can be evidenced during the same test session.…”