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Acquisition of specific response–outcome associations requires NMDA receptor activation in the basolateral amygdala but not in the insular cortex

https://doi.org/10.1016/j.nlm.2015.12.005Get rights and content

Highlights

  • We examine the acquisition of specific response–outcome (R–O) associations.

  • BLA NMDA receptor activation is required for the acquisition of R–O associations.

  • By contrast, activation of NMDA receptors in the insular cortex is not required.

Abstract

The basolateral amygdala (BLA) and the gustatory region of the insular cortex (IC) are required for the encoding and retrieval of outcome value. Here, we examined if these regions are also necessary to learn associations between actions and their outcomes. Hungry rats were first trained to press two levers for a common outcome. Next, specific response–outcome (R–O) associations were introduced such that each response now earned a distinct food outcome. Prior to each specific R–O training session, rats received a bilateral infusion of the N-methyl-d-aspartate (NMDA) receptor antagonist, DL-APV, into either the BLA or the IC. One of the two outcomes was then devalued immediately prior to a choice test. Inhibition of NMDA receptor activity in the BLA, but not the IC, during the acquisition of specific R–O associations abolished selective devaluation. These results indicate that the BLA is critical for learning the association between actions and their specific consequences.

Section snippets

Acknowledgments

This work was supported by the French ANR-14-CE13-0014 GOAL Grant awarded to EC and GF. SP was recipient of a post-doctoral fellowship from Région Aquitaine (2014) and INRA (2015–2016) and the AgreenSkills fellowship programme (2014–2016) which has received funding from the EU’s Seventh Framework Programme under Grant agreement N° FP7-267196. We thank Yoan Salafranque for the care provided to the animals during the experiments.

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      While there was indirect evidence from previous comparisons of pre- vs. post-training permanent lesions or NMDA receptor antagonism that this would be the case, our results more directly tested the effects of decreasing general neuronal function exclusively during operant training. BLA is necessary for goal-directed action in most devaluation tasks [8–10,17–22], and there is evidence that NMDA receptor blockade limited to the operant training phase can impair later devaluation in a free-operant task [22]. One research study in rats comparing the effects of pre- vs. post-training permanent lesions suggested that impairment in function during the initial acquisition phase (for Pavlovian conditioning) is sufficient to impair later devaluation if only one reinforcer is used in initial training [19].

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