Elsevier

Biological Psychiatry

Volume 67, Issue 8, 15 April 2010, Pages 737-744
Biological Psychiatry

Archival Report
Basolateral Amygdala Modulates Terminal Dopamine Release in the Nucleus Accumbens and Conditioned Responding

https://doi.org/10.1016/j.biopsych.2009.11.006Get rights and content

Background

Dopamine signaling in the nucleus accumbens (NAc) is essential for goal-directed behaviors and primarily arises from burst firing of ventral tegmental area neurons. However, the role of associative neural substrates such as the basolateral amygdala (BLA) in regulating phasic dopamine release in the NAc, particularly during reward seeking, remains unknown.

Methods

Male Sprague-Dawley rats learned to discriminate two cues: a discriminative stimulus (DS) that predicted sucrose reinforcement contingent upon a lever press and a nonassociated stimulus (NS) that predicted a second lever never reinforced with sucrose. Following training, a test session was completed in which NAc dopamine was measured using fast-scan cyclic voltammetry in conjunction with inactivation of the ipsilateral BLA (gamma-aminobutyric acid agonists; baclofen/muscimol) to determine the contribution of BLA activity to dopamine release in the NAc core during the task.

Results

Under vehicle conditions, DS and NS presentation elicited dopamine release within the NAc core. The DS evoked significantly more dopamine than the NS. Inactivation of the BLA selectively attenuated the magnitude of DS-evoked dopamine release, concurrent with an attenuation of DS-evoked conditioned approaches. Other behavioral responses (e.g., lever pressing) and dopamine release concomitant with those events were unaltered by BLA inactivation. Furthermore, neither ventral tegmental area electrically stimulated dopamine release nor the probability of high concentration dopamine release events was altered following BLA inactivation.

Conclusions

These results demonstrate that the BLA terminally modulates dopamine signals within the NAc core under specific, behaviorally relevant conditions, illustrating a functional mechanism by which the BLA selectively facilitates responding to motivationally salient environmental stimuli.

Section snippets

Subjects and Surgery

Male Sprague-Dawley rats (n = 9) (Harlan, Indianapolis, Indiana; 90–120 days; 260–350 g) were used and individually housed with a 12-hour light/12-hour dark cycle. Rats were surgically prepared for voltammetric recordings as described previously (10). A guide cannula was stereotaxically positioned above the NAc core (1.3–1.5 mm anterior, 1.3 mm lateral from bregma) and a bipolar stimulating electrode in the VTA (5.2 mm posterior, 1.0 mm lateral from bregma, 7 mm ventral from brain). A

Acquisition of Stimulus-Controlled Behavior

Rats learned the discriminative stimulus task over 8 to 12 sessions. A two-way repeated-measures ANOVA of the final six sessions revealed a significant main effect of session [F(5,60) = 12.52; p < .0001] and cue [F(1,60) = 42.69; p < .0001] on the percentage of cue trials with an operant response (Figure 1C). Post hoc comparisons revealed a significant difference between percent of cue trials with an operant response over the final 3 days of training (p < .05). The final training response

Discussion

We examined the contribution of BLA activity to NAc core dopamine during a cued sucrose reinforcement task. The DS, which predicted access to the reinforced lever, evoked significantly higher phasic dopamine than the NS, which predicted access to a nonreinforced lever. Pharmacological inactivation of the BLA selectively attenuated DS-evoked dopamine, concurrent with an attenuation of DS-evoked conditioned approaches. However, dopamine measured following NS onset, lever extensions, lever

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