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The Journal of Neuroscience, October 11, 2006, 26(41):10577-10589; doi:10.1523/JNEUROSCI.1767-06.2006

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Behavioral/Systems/Cognitive
Dopaminergic Control of Sleep–Wake States

Kafui Dzirasa,¹ Sidarta Ribeiro,¹ Rui Costa,^1,6 Lucas M. Santos,¹ Shih-Chieh Lin,¹ Andres Grosmark,¹ Tatyana D. Sotnikova,⁴ Raul R. Gainetdinov,⁴ Marc G. Caron,⁴ and Miguel A. L. Nicolelis^1,2,3,5

Departments of ¹Neurobiology, ²Biomedical Engineering, ³Psychological and Brain Sciences, and ⁴Cell Biology and ⁵Center for Neuroengineering, Duke University Medical Center, Durham, North Carolina 27710, and ⁶Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, Bethesda, Maryland 20892-9411

Correspondence should be addressed to Dr. Miguel A. L. Nicolelis, Department of Neurobiology, Duke University Medical Center, Bryan Research Building, Durham, NC 27710. Email: nicoleli{at}neuro.duke.edu

Dopamine depletion is involved in the pathophysiology of Parkinson's disease, whereas hyperdopaminergia may play a fundamental role in generating endophenotypes associated with schizophrenia. Sleep disturbances are known to occur in both schizophrenia and Parkinson's disease, suggesting that dopamine plays a role in regulating the sleep–wake cycle. Here, we show that novelty-exposed hyperdopaminergic mice enter a novel awake state characterized by spectral patterns of hippocampal local field potentials that resemble electrophysiological activity observed during rapid-eye-movement (REM) sleep. Treatment with haloperidol, a D₂ dopamine receptor antagonist, reduces this abnormal intrusion of REM-like activity during wakefulness. Conversely, mice acutely depleted of dopamine enter a different novel awake state characterized by spectral patterns of hippocampal local field potentials that resemble electrophysiological activity observed during slow-wave sleep (SWS). This dopamine-depleted state is marked by an apparent suppression of SWS and a complete suppression of REM sleep. Treatment with D₂ (but not D₁) dopamine receptor agonists recovers REM sleep in these mice. Altogether, these results indicate that dopamine regulates the generation of sleep–wake states. We propose that psychosis and the sleep disturbances experienced by Parkinsonian patients result from dopamine-mediated disturbances of REM sleep.

Key words: dopamine; sleep; REM; psychosis; schizophrenia; Parkinson's

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Received April 25, 2006; revised Aug. 29, 2006; accepted Aug. 29, 2006.

Correspondence should be addressed to Dr. Miguel A. L. Nicolelis, Department of Neurobiology, Duke University Medical Center, Bryan Research Building, Durham, NC 27710. Email: nicoleli{at}neuro.duke.edu

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