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The Journal of Neuroscience, February 11, 2009, 29(6):1735-1742; doi:10.1523/JNEUROSCI.5562-08.2009

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Behavioral/Systems/Cognitive
Synaptic Overflow of Dopamine in the Nucleus Accumbens Arises from Neuronal Activity in the Ventral Tegmental Area

Leslie A. Sombers,¹ Manna Beyene,³ Regina M. Carelli,^2,3,4 and R. Mark Wightman^1,3,4

Departments of ¹Chemistry and ²Psychology, ³Curriculum in Neurobiology, and ⁴Neuroscience Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-3290

Correspondence should be addressed to Dr. R. Mark Wightman, Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-3270. Email: rmw{at}unc.edu

Dopamine concentrations fluctuate on a subsecond time scale in the nucleus accumbens (NAc) of awake rats. These transients occur in resting animals, are more frequent following administration of drugs of abuse, and become time–locked to cues predicting reward. Despite their importance in various behaviors, the origin of these signals has not been demonstrated. Here we show that dopamine transients are evoked by neural activity in the ventral tegmental area (VTA), a brain region containing dopaminergic cell bodies. The frequency of naturally occurring dopamine transients in a resting, awake animal was reduced by a local VTA microinfusion of either lidocaine or (±)2-amino,5-phosphopentanoic acid (AP-5), an NMDA receptor antagonist that attenuates phasic firing. When dopamine increases were pharmacologically evoked by noncontingent administration of cocaine, intra-VTA infusion of lidocaine or AP-5 significantly diminished this effect. Dopamine transients acquired in response to a cue during intracranial self-stimulation were also attenuated by intra-VTA microinfusion of AP-5, and this was accompanied by an increase in latency to lever press. The results from these three distinct experiments directly demonstrate, for the first time, how neuronal firing of dopamine neurons originating in the VTA translates into synaptic overflow in a key terminal region, the NAc shell.

Key words: in vivo voltammetry; neurotransmission; carbon-fiber microelectrode; cocaine; intracranial self-stimulation; burst firing

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Received Nov. 17, 2008; revised Jan. 8, 2009; accepted Jan. 8, 2009.

Correspondence should be addressed to Dr. R. Mark Wightman, Department of Chemistry, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-3270. Email: rmw{at}unc.edu

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