Differential Expression of Motivational Stimulus Properties by Dopamine in Nucleus Accumbens Shell versus Core and Prefrontal Cortex

Abstract

The response of extracellular dopamine (DA) and its relationship to motivational valence (positive or negative) and novelty of motivational stimuli was investigated by brain microdialysis in the nucleus accumbens (NAc) shell and core and prefrontal cortex (PFCX) of rats. Stimuli were elicited by intraoral infusion of 20% sucrose, sucrose plus chocolate, quinine, and NaCl solutions, feeding of a palatable food (Fonzies), or smelling of a predator (red fox) urine. Sucrose elicited appetitive reactions and increased DA in the PFCX but not in the NAc shell. An unfamiliar appetitive taste such as that of sweet chocolate and Fonzies, increased DA in all three areas. Habituation of the stimulatory DA response to intraoral chocolate or to Fonzies feeding was observed in the NAc shell after a single pre-exposure to the same taste or food; no habituation was observed in the NAc core nor in the PFCX. Aversive taste stimuli (quinine, saturated NaCl solutions) rapidly increased DA in the PFCX and in the NAc core, and this response did not undergo one-trial habituation. In the NAc shell, instead, no effect (10 min exposure) or a delayed, transitory increase of DA (5 min exposure) sensitive to one-trial habituation was obtained in response to the aversive taste (quinine and saturated NaCl) or olfactory (red fox urine) stimuli. These observations indicate that DA responsiveness is an integrated function of the motivational valence and novelty of stimuli in the NAc shell and an expression of generic motivational value in the NAc core and PFCX.

Fig. 1.

Localization of dialysis probes (dialysing portion) within the NAc shell and core and PFCX (according to Paxinos and Watson, 1998). CPU, Caudate putamen; co, sh, core and shell of the NAc.

Fig. 2.

DA responsiveness in the PFCX and in the NAc shell to water (1 ml) and 20% sucrose solution (1 ml). Basal value: PFCX, 14 ± 1; NAc shell, 52 ± 4 (means ± SEM in femtomoles per sample). Scores of behavioral reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ● p < 0.05 with respect to basal values; *p < 0.05 with respect to the H₂O groups; ×p < 0.05 with respect to PFCX sucrose group.

Fig. 3.

Effect of pre-exposure to chocolate (1 ml) 24 hr before on DA transmission in the NAc shell and core and in the PFCX (Ringer's solution with 2.2 mm CaCl₂). Basal value: NAc shell, 56 ± 5; NAc core, 58 ± 6; PFCX, 13 ± 1 (means ± SEM in femtomoles per sample). Scores of ingestive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ●, ▴p < 0.05 with respect to basal values; *p < 0.05 with respect to naive group; ×p < 0.05 with respect to pre-exposed rats implanted in the shell; +p < 0.05 with respect to the naive group implanted in the shell and in the core.

Fig. 4.

Effect of pre-exposure to chocolate (1 ml) 24 hr before on DA transmission in the NAc shell (Ringer's solution with 1.2 mm CaCl₂). Basal value: NAc shell, 33 ± 3 (means ± SEM in femtomoles per sample). Scores of ingestive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ▪p < 0.05 with respect to basal values; *p < 0.05 with respect to naive group.

Fig. 5.

Effect of repeated Fonzies feeding during the same microdialysis session on DA output in the NAc shell and core. Latency to eat (in seconds) and amount of Fonzies eaten (in grams) are also indicated. Basal value: NAc shell, 54 ± 4; NAc core, 54 ± 5 (means ± SEM in femtomoles per sample). Results are means ± SEM of the results obtained in at least four rats. ● p < 0.05 with respect to basal values; *p < 0.05 with respect to the previous Fonzies meal.

Fig. 6.

DA responsiveness to quinine HCl 1 × 10⁻⁴m (1 ml) in the NAc shell and core and in the PFCX. Basal value: NAc shell, 54 ± 5; NAc core, 57 ± 5; PFCX, 16 ± 1 (means ± SEM in femtomoles per sample). Scores of aversive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ● p < 0.05 with respect to basal values; *p < 0.05 with respect to the group implanted in the NAc shell.

Fig. 7.

Effect of pre-exposure to quinine 5 × 10⁻⁴m (1 ml) 24 hr before on DA transmission in the NAc shell and core and in the PFCX (Ringer's solution with 2.2 mm CaCl₂). Basal value: NAc shell, 54 ± 5; NAc core, 57 ± 5; PFCX, 16 ± 1 (means ± SEM in femtomoles per sample). Scores of aversive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ●, ▴ p< 0.05 with respect to basal values; *p < 0.05 with respect to the naive group; ×p < 0.05 with respect to naive rats implanted in the NAc shell; +p < 0.05 with respect to the pre-exposed group implanted in the NAc shell.

Fig. 8.

Effect of pre-exposure to quinine 5 × 10⁻⁴m (1 ml) 24 hr before on DA transmission in the NAc shell (Ringer's solution with 1.2 mm CaCl₂). Basal value: NAc shell, 37 ± 4 (means ± SEM in femtomoles per sample). Scores of aversive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ▪ p< 0.05 with respect to basal values; *p < 0.05 with respect to the naive group.

Fig. 9.

Effect of infusion of quinine HCl 5 × 10⁻⁴m (1 ml) on DA transmission in the NAc shell of pre-exposed rats 20 min before. Basal value: NAc shell, 52 ± 5 (means ± SEM in femtomoles per sample). Scores of aversive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ● p< 0.05 with respect to basal values.

Fig. 10.

Effect of infusion of quinine HCl 5 × 10⁻⁴m (2 ml) on DA output in the NAc shell and core. Basal value: NAc shell, 56 ± 6; NAc core, 58 ± 6 (means ± SEM in femtomoles per sample). Scores of aversive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ● p < 0.05 with respect to basal values; *p < 0.05 with respect to the NAc shell group.

Fig. 11.

DA response to 0.3 m NaCl (1 ml) and NaCl saturated solution (1 ml) DA transmission in the NAc shell. Basal value: NAc shell, 54 ± 4 (means ± SEM in femtomoles per sample). Score of taste reactivity is also indicated (ingestive and aversive). Results are means ± SEM of the results obtained in at least four rats. ● p < 0.05 with respect to basal values; *p < 0.05 with respect to the NaCl 0.3 m group; #p < 0.05 with respect to the aversive score of NaCl saturated group; ×p < 0.05 with respect to the appetitive score of NaCl saturated group.

Fig. 12.

Effect of intraoral NaCl saturated solution (2 ml) DA output in the NAc shell and in the core. Basal value: NAc shell, 52 ± 5; NAc core, 56 ± 5 (means ± SEM in femtomoles per sample). Scores of aversive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ● p < 0.05 with respect to basal values; *p < 0.05 with respect to the NAc shell group.

Fig. 13.

Effect of predator odor (red fox urine) on DA transmission in the NAc shell (Ringer's solution with 1.2 mm CaCl₂). Basal value: NAc shell, 35 ± 4; NAc core, 38 ± 4; PFCX, 10 ± 1 (means ± SEM in femtomoles per sample). Scores of aversive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats. ▪ p < 0.05 with respect to basal values; *p < 0.05 with respect to NAc shell group; ×p < 0.05 with respect to NAc core group.

Fig. 14.

Effect of predator odor (red fox urine) on DA transmission in the NAc shell of pre-exposed rats 20 min before (Ringer's solution with 1.2 mm CaCl₂). Basal value: NAc shell, 35 ± 3 (means ± SEM in femtomoles per sample). Scores of aversive reactions are also indicated. Results are means ± SEM of the results obtained in at least four rats.