Neurotoxic lesions of basolateral, but not central, amygdala interfere with Pavlovian second-order conditioning and reinforcer devaluation effects

Abstract

Considerable evidence suggests that various discrete nuclei within the amygdala complex are critically involved in the assignment of emotional significance or value to events through associative learning. Much of this evidence comes from aversive conditioning procedures. For example, lesions of either basolateral amygdala (ABL) or the central nucleus (CN) interfere with the acquisition or expression of conditioned fear. The present study examined the effects of selective neurotoxic lesions of either ABL or CN on the acquisition of positive incentive value by a conditioned stimulus (CS) with two appetitive Pavlovian conditioning procedures. In second-order conditioning experiments, rats first received light-food pairings intended to endow the light with reinforcing power. The acquired reinforcing power of the light was then measured by examining its ability to serve as a reinforcer for second-order conditioning of a tone when tone-light pairings were given in the absence of food. Acquisition of second-order conditioning was impaired in rats with ABL lesions but not in rats with CN lesions. In reinforcer devaluation procedures, conditioned responding of rats with ABL lesions was insensitive to postconditioning changes in the value of the reinforcer, whereas rats with CN lesions, like normal rats, were able to spontaneously adjust their CRs to the current value of the reinforcer. The results of both test procedures indicate that ABL, but not CN, is part of a system involved in CSs' acquisition of positive incentive value. Together with evidence that identifies a role for CN in certain changes in attentional processing of CSs in conditioning, these results suggest that separate amygdala subsystems contribute to a variety of processes inherent in associative learning.

Fig. 1.

Photomicrographs showing the region of basolateral amygdala (ABL) and amygdala central nucleus (CN) in a vehicle-injected control brain (top panel) and in an ABL NMDA-lesioned brain (bottom panel). Note neuron loss and gliosis at the ABLlesion site, and sparing of neurons in CN.

Fig. 2.

First-order conditioned responses displayed by rats with basolateral amygdala lesions (ABL) and unlesioned control rats (CTL) during the light reminder trials in Phase 2 of Experiment 1A. Combined performance of the rats that received light–food pairings (Groups PP andPU) is indicated by the open bars and performance of the rats that received unpaired presentations of light and food (Group UP) is indicated by the solid bars.

Fig. 3.

Second-order conditioned responses displayed by rats with basolateral amygdala lesions (ABL) and unlesioned control rats (CTL) during tone presentations in Phase 2 of Experiment 1A. Performance of rats that received both light–food and tone–light pairings (GroupPP) is indicated by the solid symbols, and the combined performance of rats that received light–food pairings but no tone–light pairings (Group PU) and rats that received tone–light pairings but not light–food pairings (GroupUP) is indicated by the open symbols. Session P refers to the pretest of the tone at the beginning of Phase 2.

Fig. 4.

Food consumption in the taste aversion conditioning and test phases of Experiment 1B (left) and conditioned food-cup responding to the first-order light CS (right) after taste aversion training. The filled symbols and bars indicate performance of rats for which the food pellets were devalued by pairings with LiCl injections in the taste aversion conditioning phase, and theopen symbols and bars indicate performance of control rats that received unpaired presentation of food and LiCl. ABL refers to rats with basolateral amygdala lesions and CTL to unlesioned rats.

Fig. 5.

Photomicrographs showing the region of basolateral amygdala (ABL) and amygdala central nucleus (CN) in a vehicle-injected control brain (top panel) and in a CN ibotenate-lesioned brain (bottom panel). Note neuron loss and gliosis at the CNlesion site, and sparing of neurons in ABL.

Fig. 6.

First-order conditioned responses displayed by rats with central nucleus lesions (CN) and unlesioned control rats (CTL) during the light reminder trials in Phase 2 of Experiment 2A. Combined performance of the rats that received light–food pairings (Groups PP andPU) is indicated by the open bars and performance of the rats that received unpaired presentations of light and food (Group UP) is indicated by the solid bars.

Fig. 7.

Second-order conditioned responses displayed by rats with central nucleus lesions (CN) and unlesioned control rats (CTL) during tone presentations in Phase 2 of Experiment 2A. Performance of rats that received both light–food and tone–light pairings (Group PP) is indicated by the solid symbols, and the combined performance of rats that received light–food pairings but no tone–light pairings (GroupPU) and rats that received tone–light pairings but not light–food pairings (Group UP) is indicated by the open symbols. Session Prefers to the pretest of the tone at the beginning of Phase 2.

Fig. 8.

Food consumption in the taste aversion conditioning and test phases of Experiment 2B (left) and conditioned food-cup responding to the first-order light CS (right) after taste aversion training. The filled symbols and bars indicate performance of rats for which the food pellets were devalued by pairings with LiCl injections in the taste aversion conditioning phase, and theopen symbols and bars indicate performance of control rats that received unpaired presentation of food and LiCl. CN refers to rats with central nucleus lesions and CTL to unlesioned rats.