VTA dopaminergic neurons regulate ethologically relevant sleep-wake behaviors

Nature Neuroscience

Volumn 19, Issue 10, 2016, Pages 1356-1366

  Eban Rothschild, Ada ^a   Rothschild, Gideon ^b   Giardino, William J ^a   Jones, Jeff R ^a   De Lecea, Luis ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; TYROSINE 3 MONOOXYGENASE;

ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; AROUSAL; ARTICLE; CALCIUM CELL LEVEL; CHEMOGENETICS; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; FEMALE; FIBER PHOTOMETRY; GENETIC MANIPULATION; GENETIC PROCEDURES; INHIBITION (PSYCHOLOGY); MALE; MOUSE; NERVE PROJECTION; NESTING; NEUROMODULATION; NONHUMAN; NONREM SLEEP; OPTOGENETICS; PHOTOMETRY; POLYSOMNOGRAPHY; PRIORITY JOURNAL; REGULATORY MECHANISM; REM SLEEP; SALIENCE NETWORK; SLEEP INDUCTION; SLEEP WAKING CYCLE; VENTRAL TEGMENTUM; WAKEFULNESS; AMYGDALA; ANIMAL; CORPUS STRIATUM; NERVE CELL INHIBITION; NERVE TRACT; NUCLEUS ACCUMBENS; PHYSIOLOGY; PREFRONTAL CORTEX; SLEEP;

AMYGDALA; ANIMALS; CORPUS STRIATUM; DOPAMINERGIC NEURONS; MALE; MICE; NESTING BEHAVIOR; NEURAL INHIBITION; NEURAL PATHWAYS; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; SLEEP; VENTRAL TEGMENTAL AREA; WAKEFULNESS;

EID: 84987642727     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4377     Document Type: Article

References (55)

1. Robbins, T.W., & Everitt, B.J. A role for mesencephalic dopamine in activation: commentary on Berridge (2006). Psychopharmacology (Berl.) 191, 433-437 (2007).
2. Berridge, K.C., & Robinson, T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Brain Res. Rev. 28, 309-369 (1998).
3. Salamone, J.D., & Correa, M. The mysterious motivational functions of mesolimbic dopamine. Neuron 76, 470-485 (2012).
4. Wise, R.A. Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483-494 (2004).
5. Schultz, W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30, 259-288 (2007).
6. España, R.A., & Scammell, T.E. Sleep neurobiology from a clinical perspective. Sleep 34, 845-858 (2011).
7. Saper, C.B., Fuller, P.M., Pedersen, N.P., Lu, J., & Scammell, T.E. Sleep state switching. Neuron 68, 1023-1042 (2010).
8. Steinfels, G.F., Heym, J., Strecker, R.E., & Jacobs, B.L. Behavioral correlates of dopaminergic unit activity in freely moving cats. Brain Res. 258, 217-228 (1983).
9. Trulson, M.E., & Preussler, D.W. Dopamine-containing ventral tegmental area neurons in freely moving cats: activity during the sleep-waking cycle and effects of stress. Exp. Neurol. 83, 367-377 (1984).
10. Trulson, M.E., Preussler, D.W., & Howell, G.A. Activity of substantia nigra units across the sleep-waking cycle in freely moving cats. Neurosci. Lett. 26, 183-188 (1981).
11. Miller, J.D., Farber, J., Gatz, P., Roffwarg, H., & German, D.C. Activity of mesencephalic dopamine and non-dopamine neurons across stages of sleep and walking in the rat. Brain Res. 273, 133-141 (1983).
12. Jones, B.E., Bobillier, P., Pin, C., & Jouvet, M. The effect of lesions of catecholamine-containing neurons upon monoamine content of the brain and EEG and behavioral waking in the cat. Brain Res. 58, 157-177 (1973).
13. Boutrel, B., & Koob, G.F. What keeps us awake: the neuropharmacology of stimulants and wakefulness-promoting medications. Sleep 27, 1181-1194 (2004).
14. Wisor, J.P., et al. Dopaminergic role in stimulant-induced wakefulness. J. Neurosci. 21, 1787-1794 (2001).
15. Qu, W.M., Huang, Z.L., Xu, X.H., Matsumoto, N., & Urade, Y. Dopaminergic D1 and D2 receptors are essential for the arousal effect of modafinil. J. Neurosci. 28, 8462-8469 (2008).
16. Holst, S.C., et al. Dopaminergic role in regulating neurophysiological markers of sleep homeostasis in humans. J. Neurosci. 34, 566-573 (2014).
17. Dzirasa, K., et al. Dopaminergic control of sleep-wake states. J. Neurosci. 26, 10577-10589 (2006).
18. Qu, W.M., et al. Essential role of dopamine D2 receptor in the maintenance of wakefulness, but not in homeostatic regulation of sleep, in mice. J. Neurosci. 30, 4382-4389 (2010).
19. Monti, J.M., & Monti, D. The involvement of dopamine in the modulation of sleep and waking. Sleep Med. Rev. 11, 113-133 (2007).
20. Zhou, Q.Y., & Palmiter, R.D. Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell 83, 1197-1209 (1995).
21. Ungerstedt, U. Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol. Scand. Suppl. 367, 95-122 (1971).
22. Léna, I., et al. Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep-wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats. J. Neurosci. Res. 81, 891-899 (2005).
23. Dahan, L., et al. Prominent burst firing of dopaminergic neurons in the ventral tegmental area during paradoxical sleep. Neuropsychopharmacology 32, 1232-1241 (2007).
24. Gunaydin, L.A., et al. Natural neural projection dynamics underlying social behavior. Cell 157, 1535-1551 (2014).
25. Lerner, T.N., et al. Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits. Cell 162, 635-647 (2015).
26. Alexander, G.M., et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron 63, 27-39 (2009).
27. Hediger, H. Comparative observations on sleep. Proc. R. Soc. Med. 62, 153-156 (1969).
28. Meddis, R. On the function of sleep. Anim. Behav. 23, 676-691 (1975).
29. Moruzzi, G. Sleep and instinctive behavior. Arch. Ital. Biol. 107, 175-216 (1969).
30. Gaskill, B.N., et al. Heat or insulation: behavioral titration of mouse preference for warmth or access to a nest. PLoS One 7, e32799 (2012).
31. Curie, T., et al. Homeostatic and circadian contribution to EEG and molecular state variables of sleep regulation. Sleep 36, 311-323 (2013).
32. Burgess, C.R., Tse, G., Gillis, L., & Peever, J.H. Dopaminergic regulation of sleep and cataplexy in a murine model of narcolepsy. Sleep 33, 1295-1304 (2010).
33. Brown, R.E., Basheer, R., McKenna, J.T., Strecker, R.E., & McCarley, R.W. Control of sleep and wakefulness. Physiol. Rev. 92, 1087-1187 (2012).
34. Lu, J., Jhou, T.C., & Saper, C.B. Identification of wake-Active dopaminergic neurons in the ventral periaqueductal gray matter. J. Neurosci. 26, 193-202 (2006).
35. Hall, Z.J., Healy, S.D., & Meddle, S.L. A role for nonapeptides and dopamine in nest-building behaviour. J. Neuroendocrinol. 27, 158-165 (2015).
36. Lazarus, M., Chen, J.F., Urade, Y., & Huang, Z.L. Role of the basal ganglia in the control of sleep and wakefulness. Curr. Opin. Neurobiol. 23, 780-785 (2013).
37. Qiu, M.H., et al. The role of nucleus accumbens core/shell in sleep-wake regulation and their involvement in modafinil-induced arousal. PLoS One 7, e45471 (2012).
38. Andretic, R., van Swinderen, B., & Greenspan, R.J. Dopaminergic modulation of arousal in Drosophila. Curr. Biol. 15, 1165-1175 (2005).
39. Kume, K., Kume, S., Park, S.K., Hirsh, J., & Jackson, F.R. Dopamine is a regulator of arousal in the fruit fly. J. Neurosci. 25, 7377-7384 (2005).
40. Pimentel, D., et al. Operation of a homeostatic sleep switch. Nature http://dx.doi.org/10.1038/nature19055 (2016).
41. Salamone, J.D., Cousins, M.S., & Snyder, B.J. Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis. Neurosci. Biobehav. Rev. 21, 341-359 (1997).
42. Zhang, F., et al. Optogenetics in freely moving mammals: dopamine and reward. Cold Spring Harb. Protoc. http://dx.doi.org/10.1101/pdb.top086330 (2015).
43. Adamantidis, A.R., et al. Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J. Neurosci. 31, 10829-10835 (2011).
44. Tye, K.M., et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493, 537-541 (2013).
45. Chaudhury, D., et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493, 532-536 (2013).
46. Danjo, T., Yoshimi, K., Funabiki, K., Yawata, S., & Nakanishi, S. Aversive behavior induced by optogenetic inactivation of ventral tegmental area dopamine neurons is mediated by dopamine D2 receptors in the nucleus accumbens. Proc. Natl. Acad. Sci. USA 111, 6455-6460 (2014).
47. Cousins, D.A., Butts, K., & Young, A.H. The role of dopamine in bipolar disorder. Bipolar Disord. 11, 787-806 (2009).
48. Wulff, K., Gatti, S., Wettstein, J.G., & Foster, R.G. Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nat. Rev. Neurosci. 11, 589-599 (2010).
49. Parekh, P.K., Ozburn, A.R., & McClung, C.A. Circadian clock genes: effects on dopamine, reward and addiction. Alcohol 49, 341-349 (2015).
50. Winton-Brown, T.T., Fusar-Poli, P., Ungless, M.A., & Howes, O.D. Dopaminergic basis of salience dysregulation in psychosis. Trends Neurosci. 37, 85-94 (2014).
51. Deacon, R.M. Assessing nest building in mice. Nat. Protoc. 1, 1117-1119 (2006).
52. Palchykova, S., Winsky-Sommerer, R., Meerlo, P., Dürr, R., & Tobler, I. Sleep deprivation impairs object recognition in mice. Neurobiol. Learn. Mem. 85, 263-271 (2006).
53. Anaclet, C., et al. The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nat. Neurosci. 17, 1217-1224 (2014).
54. Carter, M.E., et al. Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat. Neurosci. 13, 1526-1533 (2010).
55. Jego, S., et al. Optogenetic identification of a rapid eye movement sleep modulatory circuit in the hypothalamus. Nat. Neurosci. 16, 1637-1643 (2013).