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The nucleus accumbens (NAc) receives converging input from a number of structures proposed to play a role in affective disorders. In particular, the basolateral amygdala (BLA) provides an affective input that overlaps with context-related information derived from the ventral subiculum of the hippocampus (vSub). We examined how stimulation of the BLA is modulated by, and in turn affects, vSub inputs to this region. In-vivo extracellular recordings were performed in the NAc of anaesthetized rats. The effect of high-frequency (theta-burst) stimulation (HFS) of the BLA on both BLA and vSub-evoked responses was tested. In addition, the involvement of dopamine D2 receptors in BLA-induced plasticity in the NAc was examined by pre-treatment with sulpiride (5 mg/kg i.v.). Finally, tetrodotoxin (TTX) was used to inactivate the vSub and the effect on BLA-evoked responses was assessed. We found that HFS of the BLA causes hetereogeneous patterns of plasticity, depression and potentiation, respectively, in the rostral and caudal subregions of the NAc that are disrupted following D2 receptor antagonist treatment. In addition, inactivating the vSub with TTX attenuates the ability of the BLA to drive spike firing in the NAc. Thus, the vSub is required for activation of the NAc by the BLA. These data support a model whereby the amygdala can coordinate reward-seeking and fear-related behaviours via its differential regulation of NAc output. In addition, the hippocampus inappropriately dominates information processing within this circuit, potentially contributing to the overwhelming focus on internal emotional states in disorders such as depression.

Heterogeneous processing of amygdala and hippocampal inputs in the rostral and caudal subregions of the nucleus accumbens