ABSTRACT
BACKGROUND: While studies suggest that both dopamine and norepinephrine neurotransmission support reinforcement learning, the role of dopamine has been emphasized. As a result, little is known about norepinephrine signaling during reward learning and extinction. Both dopamine and norepinephrine projections innervate distinct regions of the bed nucleus of the stria terminalis (BNST), a structure that mediates behavioral and autonomic responses to stress and anxiety. We investigated whether norepinephrine release in the ventral BNST (vBNST) and dopamine release in the dorsolateral BNST (dlBNT) correlate with reward learning during intracranial self-stimulation (ICSS). METHODS: Using fast-scan cyclic voltammetry, norepinephrine concentration changes in the vBNST (n = 12 animals) during ICSS were compared with dopamine changes in the dlBNST (n = 7 animals) and nucleus accumbens (NAc) (n = 5 animals). Electrical stimulation was in the ventral tegmental area/substantia nigra region. RESULTS: Whereas dopamine release was evoked by presentation of a cue predicting reward availability in both dlBNST and NAc, cue-evoked norepinephrine release did not occur in the vBNST. Release of both catecholamines was evoked by the electrical stimulation. Extracellular changes in norepinephrine were also studied during extinction of ICSS and compared with results obtained for dopamine. During extinction of ICSS, norepinephrine release in the vBNST occurred at the time where the stimulation was anticipated, whereas dopamine release transiently decreased. CONCLUSIONS: The data demonstrate that norepinephrine release in the vBNST differs from dopamine release in the dlBNST and the NAc in that it signals the absence of reward rather than responding to reward predictive cues.
Subject(s)
Dopamine/metabolism , Extinction, Psychological/physiology , Norepinephrine/metabolism , Nucleus Accumbens/physiology , Reward , Self Stimulation/physiology , Septal Nuclei/physiology , Adrenergic Uptake Inhibitors/pharmacology , Animals , Desipramine/pharmacology , Dopamine Uptake Inhibitors/pharmacology , Male , Nucleus Accumbens/metabolism , Piperazines/pharmacology , Rats , Rats, Sprague-Dawley , Septal Nuclei/metabolismABSTRACT
BACKGROUND: Traditionally, norepinephrine has been associated with stress responses, whereas dopamine has been associated with reward. Both of these catecholamines are found within the bed nucleus of the stria terminalis (BNST), a brain relay nucleus in the extended amygdala between cortical/limbic centers, and the hypothalamic-pituitary-adrenal axis. Despite this colocalization, little is known about subsecond catecholamine signaling in subregions of the BNST in response to salient stimuli. METHODS: Changes in extracellular catecholamine concentration in subregions of the BNST in response to salient stimuli were measured within the rat BNST with fast-scan cyclic voltammetry at carbon-fiber microelectrodes. RESULTS: A discrete subregional distribution of release events was observed for different catecholamines in this nucleus. In addition, rewarding and aversive tastants evoked inverse patterns of norepinephrine and dopamine release in the BNST. An aversive stimulus, quinine, activated noradrenergic signaling but inhibited dopaminergic signaling, whereas a palatable stimulus, sucrose, inhibited norepinephrine while causing dopamine release. CONCLUSIONS: This reciprocal relationship, coupled with their different time courses, can provide integration of opposing hedonic states to influence response outputs appropriate for survival.