Differential influence of associative and nonassociative learning mechanisms on the responsiveness of prefrontal and accumbal dopamine transmission to food stimuli in rats fed ad libitum

Abstract

Feeding a novel food (Fonzies) to rats fed ad libitum with standard food increased extracellular dopamine (DA) in the medial prefrontal cortex (PFCX) and in the medial nucleus accumbens (NAc). Previous Fonzies feeding, although it did not affect the increase of extracellular DA in the PFCX in response to Fonzies feeding, blunted that increase in the NAc (habituation); recovery from habituation in the NAc was complete 5 d after previous Fonzies feeding. Predictive association of an otherwise neutral stimulus extrinsic to Fonzies (empty plastic box) with Fonzies feeding resulted in the acquisition by the stimulus of the property to elicit incentive responses directed toward the stimulus and to increase extracellular DA in the PFCX. However, the same stimulus, or a more complex stimulus including intrinsic stimuli (Fonzies-filled plastic box), failed to acquire the ability to modify extracellular DA in the NAc. Pseudoconditioning, i.e., nonpredictive association of the extrinsic stimulus (empty box) with Fonzies feeding, did not result in acquisition by the stimulus of the property to elicit incentive responses and to increase extracellular DA in the PFCX. Repeated nonreinforced presentation of previously conditioned extrinsic stimuli (empty box) resulted in extinction of the property to elicit incentive responses and to increase extracellular DA in the PFCX. These results indicate that in rats fed ad libitum, phasic activation of mesocortical and mesolimbic DA systems by motivational stimuli is differentially influenced by associative (conditioning) and nonassociative (habituation) learning mechanisms and is differentially related to acquisition and expression of incentive motivation.

Fig. 1.

Effect of Fonzies feeding on DA output in dialysates from the PFCX (top) and the NAc (bottom) of Fonzies-naive and Fonzies-trained rats. Latency to eat (in seconds) and amount of Fonzies eaten (in grams) are also shown. Results are mean ± SEM of the results obtained in at least four rats. Filled symbols, p< 0.05 with respect to basal values; *p < 0.05 with respect to Fonzies-naive rats.

Fig. 2.

Schematic representation (according to Paxinos and Watson, 1987) of the areas implanted with vertical dialysis probes. Indicated is the placement of the probes of Experiment 1, the results of which are shown in Figure 1 (Fonzies-naive). cc, Corpus callosum; ca, anterior commissure;Cl, claustrum; CPU, caudate putamen;Co, core; Sh, shell of the nucleus accumbens.

Fig. 3.

Effect of repeated Fonzies feeding during the same microdialysis session on DA output in dialysates from the PFCX (top) and the NAc (bottom). Latency to eat (in seconds) and amount of Fonzies eaten (in grams) are also indicated. Results are mean ± SEM of results obtained in at least four rats. Filled symbols, p < 0.05 with respect to basal values; *p < 0.05 with respect to the previous Fonzies meal.

Fig. 4.

Effect of previous Fonzies feeding on DA output in dialysates from the NAc. Three groups were compared: naive, fed on Fonzies 1 d before, or fed on Fonzies 5 d before. Latency to eat (in seconds) and amount of Fonzies eaten (in grams) are also indicated. Results are mean ± SEM of results obtained in at least four rats. Filled symbols, p < 0.05 with respect to basal values; *p < 0.05 with respect to Fonzies-naive; ^#p < 0.05 with respect to rats fed on Fonzies 1 d before the experiment.

Fig. 5.

Time course of incentive behavior. Behavior was scored in blocks of 5 min, after presentation of an extrinsic stimulus (empty plastic box) to rats of the conditioned, unconditioned, pseudoconditioned, and extinction groups of Experiment 5, and after presentation of a combined, intrinsic–extrinsic stimulus (Fonzies-filled plastic box) to conditioned rats of Experiment 6. Results are mean ± SEM of results obtained in at least four rats. *p < 0.05 with respect to basal values;^#p < 0.05 with respect to unconditioned, pseudoconditioned, and extinction. Filled symbols, p < 0.05 with respect to conditioned to empty plastic box.

Fig. 6.

Effect of presentation of a conditioned extrinsic stimulus (empty plastic box) and of Fonzies feeding on DA output in dialysates from the PFCX. Four groups were compared: conditioned, unconditioned, pseudoconditioned, and extinction. Incentive score, latency to eat, and amount of Fonzies eaten are also indicated. Results are mean ± SEM of results obtained in at least four rats. Filled symbols, p < 0.05 with respect to basal values; *p < 0.05 with respect to the unconditioned, pseudoconditioned, and extinction groups.

Fig. 7.

Effect of Fonzies feeding on DA output in dialysates from the NAc of conditioned and unconditioned rats. Incentive score, latency to eat (in seconds), and amount of Fonzies eaten are also indicated. Results are mean ± SEM of results obtained in at least four rats. Filled symbols,p < 0.05 with respect to basal values; *p < 0.05 with respect to unconditioned.

Fig. 8.

Effect of presentation of a conditioned combined (intrinsic–extrinsic) stimulus (Fonzies-filled plastic box) and of Fonzies feeding on DA output in dialysate from the PFCX (top) and the NAc (bottom). Incentive score, latency to eat, and amount of Fonzies eaten are also indicated. Results are mean ± SEM of results obtained in at least four rats.Filled symbols, p < 0.05 with respect to basal values.