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The Journal of Neuroscience, April 1, 2009, 29(13):4035-4043; doi:10.1523/JNEUROSCI.0261-09.2009

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Behavioral/Systems/Cognitive
Dopamine Signaling Differences in the Nucleus Accumbens and Dorsal Striatum Exploited by Nicotine

Tianxiang Zhang,^1 * Lifen Zhang,^1 * Yong Liang,¹ Athanassios G. Siapas,³ Fu-Ming Zhou,⁴ and John A. Dani^1,2

¹Department of Neuroscience and ²Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, Texas 77030, ³Division of Biology, California Institute of Technology, Pasadena, California 91125, and ⁴Department of Pharmacology, University of Tennessee, Memphis, Tennessee 38163

Correspondence should be addressed to John A. Dani, Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030-3498. Email: jdani{at}bcm.tmc.edu

The dorsal striatum and the nucleus accumbens (NAc) shell of the ventral striatum have similar cellular components and are both richly innervated by dopamine neurons. Despite similarities that extend throughout the striatum, only the NAc shell has a conspicuous increase in basal dopamine upon the initial administration of psychostimulant drugs such as nicotine. As measured by microdialysis, the elevated dopamine in the NAc shell is considered an identifying functional characteristic of addictive drugs. To examine this general functional difference between nicotine's action on the dorsolateral striatum and NAc shell, we directly monitored dopamine release in rat striatal slices using fast-scan cyclic voltammetry. In addition, we separately monitored the in vivo unit firing activity of putative midbrain dopamine neurons from freely moving rats using chronic multiple tetrodes. Nicotine administration increased the firing frequency of dopamine neurons and specifically increased the number and the length of phasic burst firing. The frequency dependence for dopamine release in the dorsolateral striatum and NAc shell is fundamentally different, enabling mainly the NAc shell to capitalize on the nicotine-induced phasic burst firing by dopamine neurons. Although nicotine decreased low-frequency (tonic) dopamine release in both areas, the increased ratio of phasic bursts relative to tonic firing caused by nicotine boosted the basal dopamine concentration predominantly in the NAc shell. By favoring release from bursts while depressing release from tonic signals, nicotine spreads the range of dopamine signaling and effectively increases the signal-to-noise relationship along dopamine afferents.

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Received Jan. 16, 2009; accepted Feb. 25, 2009.

Correspondence should be addressed to John A. Dani, Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030-3498. Email: jdani{at}bcm.tmc.edu

This article has been cited by other articles:

				L. Zhang, W. M. Doyon, J. J. Clark, P. E. M. Phillips, and J. A. Dani Controls of Tonic and Phasic Dopamine Transmission in the Dorsal and Ventral Striatum Mol. Pharmacol., August 1, 2009; 76(2): 396 - 404. [Abstract] [Full Text] [PDF]

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