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The Journal of Neuroscience, May 16, 2007, 27(20):5414-5421; doi:10.1523/JNEUROSCI.5347-06.2007

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Behavioral/Systems/Cognitive
Functional Coupling between the Prefrontal Cortex and Dopamine Neurons in the Ventral Tegmental Area

Ming Gao,¹ Chang-Liang Liu,¹ Shen Yang,¹ Guo-Zhang Jin,¹ Benjamin S. Bunney,² and Wei-Xing Shi^1,2

¹Department of Pharmacology, Shanghai Institute of Materia Medica, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 201203, China, and ²Neuropsychopharmacological Research Unit, Department of Psychiatry, Yale University School of Medicine, New Haven, Connecticut 06511

Correspondence should be addressed to Dr. Wei-Xing Shi, Neuropsychopharmacological Research Unit, Yale University School of Medicine, 300 George Street, Room 8300C, New Haven, CT 06511. Email: wei-xing.shi{at}yale.edu

Stimulation of the prefrontal cortex (PFC) has been shown to have an excitatory influence on dopamine (DA) neurons. We report here that, under nonstimulated conditions, the activity of DA neurons in the ventral tegmental area (VTA) also covaries, on a subsecond timescale, with the activity of PFC cells. Thus, in 67% of VTA DA neurons recorded in chloral hydrate-anesthetized rats, the firing of the cell displayed a slow oscillation (SO) that was highly coherent with the activity of PFC neurons. The SO was suppressed by transections immediately caudal to the PFC or by intra-PFC infusion of tetrodotoxin, suggesting that it depends on inputs derived from the PFC. Unexpectedly, the SO in most VTA DA neurons was reversed in phase relative to PFC cell activity, suggesting that at least part of PFC information is transferred to DA neurons indirectly through inhibitory relay neurons. These results, together with those reported previously, suggest that the PFC can act through multiple pathways to exert both excitatory and inhibitory influences on DA neurons. The observed functional coupling between DA and PFC neurons further suggests that these pathways not only allow a bidirectional control of DA neurons by the PFC, but also enable action potential-dependent DA release to be coordinated, on a subsecond timescale, with glutamate release from PFC terminals. Further understanding of this coordinated activity may provide important new insights into brain functions and disorders thought to involve both VTA DA and PFC neurons.

Key words: prefrontal cortex; ventral tegmental area; dopamine neuron; firing pattern; slow oscillation; bursting

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Received Dec. 12, 2006; revised March 25, 2007; accepted April 16, 2007.

Correspondence should be addressed to Dr. Wei-Xing Shi, Neuropsychopharmacological Research Unit, Yale University School of Medicine, 300 George Street, Room 8300C, New Haven, CT 06511. Email: wei-xing.shi{at}yale.edu

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