2,070
Views
7
CrossRef citations to date
0
Altmetric
Review

How genetically engineered systems are helping to define, and in some cases redefine, the neurobiological basis of sleep and wake

, &
Pages 406-417 | Received 22 May 2015, Accepted 15 Jul 2015, Published online: 12 Oct 2015

References

  • Kohtoh S, Taguchi Y, Matsumoto N, Wada M, Huang Z-L, Urade Y. Algorithm for sleep scoring in experimental animals based on fast Fourier transform power spectrum analysis of the electroencephalogram. Sleep Biol Rhythms 2008; 6:163-71; http://dx.doi.org/10.1111/j.1479-8425.2008.00355.x
  • Tobler I, Deboer T, Fischer M. Sleep and Sleep Regulation in Normal and Prion Protein-Deficient Mice. J Neurosci 1997; 17:1869-79; PMID:9030645
  • Oishi Y, Takata Y, Urade Y, Lazarus M. Polygraphic recordings to measure sleep in mice. J Vis Exp 2015: in press.
  • Rosenbaum E. Warum müssen wir schlafen? : eine neue Theorie des Schlafes. Berlin: August Hirschwald, 1892.
  • Kubota K. Kuniomi Ishimori and the first discovery of sleep-inducing substances in the brain. Neurosci Res 1989; 6:497-518; PMID:2677843; http://dx.doi.org/10.1016/0168-0102(89)90041-2
  • Ishimori K. True cause of sleep: a hypnogenic substance as evidenced in the brain of sleep-deprived animals. Tokyo Igakkai Zasshi 1909; 23:429-57
  • Legendre R, Pieron H. Recherches sur le besoin de sommeil consécutif à une veille prolongée. Z Allegem Physiol 1913; 14:235-62
  • Inoué S, Honda K, Komoda Y. Sleep as neuronal detoxification and restitution. Behav Brain Res 1995; 69:91-6; http://dx.doi.org/10.1016/0166-4328(95)00014-K
  • Urade Y, Hayaishi O. Prostaglandin D2 and sleep/wake regulation. Sleep Med Rev 2011; 15:411-8; PMID:22024172; http://dx.doi.org/10.1016/j.smrv.2011.08.003
  • Ueno R, Ishikawa Y, Nakayama T, Hayaishi O. Prostaglandin D2 induces sleep when microinjected into the preoptic area of conscious rats. Biochem Biophys Res Commun 1982; 109:576-82; PMID:6960896; http://dx.doi.org/10.1016/0006-291X(82)91760-0
  • Urade Y, Lazarus M. Prostaglandin D2 in the regulation of sleep. In: Shaw PJ, Tafti M, Thorpy MJ, eds. The Genetic Basis of Sleep and Sleep Disorders. New York: Cambridge University, 2013:73-83.
  • Krueger JM, Walter J, Dinarello CA, Wolff SM, Chedid L. Sleep-promoting effects of endogenous pyrogen (interleukin-1). Am J Physiol 1984; 246:R994-9; PMID:6611091
  • Krueger JM, Clinton JM, Winters BD, Zielinski MR, Taishi P, Jewett KA, Davis CJ. Involvement of cytokines in slow wave sleep. Prog Brain Res 2011; 193:39-47; PMID:21854954; http://dx.doi.org/10.1016/B978-0-444-53839-0.00003-X
  • Porkka-Heiskanen T, Strecker RE, Thakkar M, Bjorkum AA, Greene RW, McCarley RW. Adenosine: a mediator of the sleep-inducing effects of prolonged wakefulness. Science 1997; 276:1265-8; PMID:9157887; http://dx.doi.org/10.1126/science.276.5316.1265
  • Porkka-Heiskanen T, Kalinchuk AV. Adenosine, energy metabolism and sleep homeostasis. Sleep Med Rev 2011; 15:123-35; PMID:20970361; http://dx.doi.org/10.1016/j.smrv.2010.06.005
  • Garcia-Garcia F, Acosta-Pena E, Venebra-Munoz A, Murillo-Rodriguez E. Sleep-inducing factors. CNS Neurol Disord Drug Targets 2009; 8:235-44; PMID:19689305; http://dx.doi.org/10.2174/187152709788921672
  • Huitron-Resendiz S, Kristensen MP, Sánchez-Alavez M, Clark SD, Grupke SL, Tyler C, Suzuki C, Nothacker H-P, Civelli O, Criado JR, et al. Urotensin II Modulates Rapid Eye Movement Sleep through Activation of Brainstem Cholinergic Neurons. J Neurosci 2005; 25:5465-74; PMID:15944374; http://dx.doi.org/10.1523/JNEUROSCI.4501-04.2005
  • Saper CB, Romanovsky AA, Scammell TE. Neural circuitry engaged by prostaglandins during the sickness syndrome. Nat Neurosci 2012; 15:1088-95; PMID:22837039; http://dx.doi.org/10.1038/nn.3159
  • Krueger JM, Obal F, Jr, Fang J, Kubota T, Taishi P. The Role of Cytokines in Physiological Sleep Regulation. Ann NY Acad Sci 2001; 933:211-21; PMID:12000022; http://dx.doi.org/10.1111/j.1749-6632.2001.tb05826.x
  • Krueger JM, Majde JA. Humoral Links between Sleep and the Immune System: Research Issues. Ann NY Acad Sci 2003; 992:9-20; PMID:12794042
  • Mullington JM, Hinze-Selch D, Pollmacher T. Mediators of inflammation and their interaction with sleep: relevance for chronic fatigue syndrome and related conditions. Ann NY Acad Sci 2001; 933:201-10; PMID:12000021; http://dx.doi.org/10.1111/j.1749-6632.2001.tb05825.x
  • Mullington J, Korth C, Hermann DM, Orth A, Galanos C, Holsboer F, Pollmächer T. Dose-dependent effects of endotoxin on human sleep. Am J Physiol Regul Integr Comp Physiol 2000; 278:R947-55; PMID:10749783
  • Oishi Y, Yoshida K, Scammell TE, Urade Y, Lazarus M, Saper CB. The roles of prostaglandin E2 and D2 in lipopolysaccharide-mediated changes in sleep. Brain Behav Immun 2015; 47:172-7; PMID:25532785; http://dx.doi.org/10.1016/j.bbi.2014.11.019
  • Ushikubi F, Segi E, Sugimoto Y, Murata T, Matsuoka T, Kobayashi T, Hizaki H, Tuboi K, Katsuyama M, Ichikawa A, et al. Impaired febrile response in mice lacking the prostaglandin E receptor subtype EP3. Nature 1998; 395:281-24; PMID:9751056; http://dx.doi.org/10.1038/26233
  • Lazarus M, Yoshida K, Coppari R, Bass CE, Mochizuki T, Lowell BB, Saper CB. EP3 prostaglandin receptors in the median preoptic nucleus are critical for fever responses. Nat Neurosci 2007; 10:1131-3; PMID:17676060; http://dx.doi.org/10.1038/nn1949
  • Wilkins RH, Brody IA. ENcephalitis lethargica. Arch Neurol 1968; 18:324-8; PMID:4868286; http://dx.doi.org/10.1001/archneur.1968.00470330114013
  • von Economo C. Die Encephalitis lethargica. Wien Klin Wochenschr 1917; 30:581-5
  • Economo CV. Sleep as a problem of localization. J Nerv Ment Dis 1930; 71:249-59; http://dx.doi.org/10.1097/00005053-193003000-00001
  • Ranson SW. SOmnolence caused by hypothalamic lesions in the monkey. Arch Neurol Psychiatry 1939; 41:1-23; http://dx.doi.org/10.1001/archneurpsyc.1939.02270130011001
  • Moruzzi G, Magoun HW. Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1949; 1:455-73; PMID:18421835; http://dx.doi.org/10.1016/0013-4694(49)90219-9
  • Saper CB, Fuller PM, Pedersen NP, Lu J, Scammell TE. Sleep State Switching. Neuron 2010; 68:1023-42; PMID:21172606; http://dx.doi.org/10.1016/j.neuron.2010.11.032
  • Brown RE, Basheer R, McKenna JT, Strecker RE, McCarley RW. Control of Sleep and Wakefulness. Physiol Rev 2012; 92:1087-187; PMID:22811426; http://dx.doi.org/10.1152/physrev.00032.2011
  • Fuller PM, Gooley JJ, Saper CB. Neurobiology of the Sleep-Wake Cycle: Sleep Architecture, Circadian Regulation, and Regulatory Feedback. J Biol Rhythms 2006; 21:482-93; PMID:17107938; http://dx.doi.org/10.1177/0748730406294627
  • Jones BE. Activity, modulation and role of basal forebrain cholinergic neurons innervating the cerebral cortex. Prog Brain Res 2004;145:157-69; PMID: 14650914; http://dx.doi.org/10.1016/S0079-6123(03)45011-5
  • Blanco-Centurion C, Xu M, Murillo-Rodriguez E, Gerashchenko D, Shiromani AM, Salin-Pascual RJ, Hof PR, Shiromani PJ. Adenosine and Sleep Homeostasis in the Basal Forebrain. J Neurosci 2006; 26:8092-100; PMID:16885223; http://dx.doi.org/10.1523/JNEUROSCI.2181-06.2006
  • Kapás L, Obál Jr F, Book AA, B. Schweitzer J, Wiley RG, Krueger JM. The effects of immunolesions of nerve growth factor-receptive neurons by 192 IgG-saporin on sleep. Brain Res 1996; 712:53-9; http://dx.doi.org/10.1016/0006-8993(95)01431-4
  • Saper CB, Scammell TE, Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature 2005; 437:1257-63; PMID:16251950; http://dx.doi.org/10.1038/nature04284
  • Fort P, Bassetti CL, Luppi PH. Alternating vigilance states: new insights regarding neuronal networks and mechanisms. Eur J Neurosci 2009; 29:1741-53; PMID:19473229; http://dx.doi.org/10.1111/j.1460-9568.2009.06722.x
  • Lin L, Faraco J, Li R, Kadotani H, Rogers W, Lin X, Qiu X, de Jong PJ, Nishino S, Mignot E. The sleep disorder canine narcolepsy is caused by a mutation in the hypocretin (orexin) receptor 2 gene. Cell 1999; 98:365-76; PMID:10458611; http://dx.doi.org/10.1016/S0092-8674(00)81965-0
  • Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, Richardson JA, Williams SC, Xiong Y, Kisanuki Y, et al. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 1999; 98:437-51; PMID:10481909; http://dx.doi.org/10.1016/S0092-8674(00)81973-X
  • Thannickal TC, Moore RY, Nienhuis R, Ramanathan L, Gulyani S, Aldrich M, Cornford M, Siegel JM. Reduced number of hypocretin neurons in human narcolepsy. Neuron 2000; 27:469-74; PMID:11055430; http://dx.doi.org/10.1016/S0896-6273(00)00058-1
  • Lu J, Sherman D, Devor M, Saper CB. A putative flip–flop switch for control of REM sleep. Nature 2006; 441:589-94; PMID:16688184; http://dx.doi.org/10.1038/nature04767
  • Fuller PM, Saper CB, Lu J. The pontine REM switch: past and present. J Physiol (Lond) 2007; 584:735-41; PMID:17884926; http://dx.doi.org/10.1113/jphysiol.2007.140160
  • Murphy PJ, Campbell SS. Nighttime drop in body temperature: a physiological trigger for sleep onset? Sleep 1997; 20:505-11; PMID:9322266
  • Raymann RJ, Swaab DF, Van Someren EJ. Skin deep: enhanced sleep depth by cutaneous temperature manipulation. Brain 2008; 131:500-13; PMID:18192289; http://dx.doi.org/10.1093/brain/awm315
  • Romanovsky AA. Thermoregulation: some concepts have changed. Functional architecture of the thermoregulatory system. Am J Physiol Regul Integr Comp Physiol 2007; 292:R37-46; PMID:17008453; http://dx.doi.org/10.1152/ajpregu.00668.2006
  • Szymusiak R, McGinty D. Hypothalamic regulation of sleep and arousal. Ann NY Acad Sci 2008; 1129:275-86; PMID:18591488; http://dx.doi.org/10.1196/annals.1417.027
  • Fuller P, Sherman D, Pedersen NP, Saper CB, Lu J. Reassessment of the structural basis of the ascending arousal system. J Comp Neurol 2011; 519:3817-; http://dx.doi.org/10.1002/cne.22781
  • Kaur S, Pedersen NP, Yokota S, Hur EE, Fuller PM, Lazarus M, Chamberlin NL, Saper CB. Glutamatergic Signaling from the Parabrachial Nucleus Plays a Critical Role in Hypercapnic Arousal. J Neurosci 2013; 33:7627-40; PMID:23637157; http://dx.doi.org/10.1523/JNEUROSCI.0173-13.2013
  • Nakamura K, Morrison SF. A thermosensory pathway that controls body temperature. Nat Neurosci 2008; 11:62-71; PMID:18084288; http://dx.doi.org/10.1038/nn2027
  • Chen R-F, Lee C-Y. Adenoviruses Types, Cell Receptors and Local Innate Cytokines in Adenovirus Infection. Int Rev Immunol 2014; 33:45-53; PMID:24127823; http://dx.doi.org/10.3109/08830185.2013.823420
  • Lopez-Huerta V, Nakano Y, Bausenwein J, Jaidar O, Lazarus M, Cherassse Y, Garcia-Munoz M, Arbuthnott G. The neostriatum: two entities, one structure? Brain Struct Funct 2015; PMID:25652680; http://dx.doi.org/10.1007/s00429-015-1000-4
  • Yazaki-Sugiyama Y, Yanagihara S, Fuller PM, Lazarus M. Acute inhibition of a cortical motor area impairs vocal control in singing zebra finches. Eur J Neurosci 2014: 41(1):97-108; PMID:25354166; http://dx.doi.org/10.1111/ejn.12757
  • Lewandoski M. Conditional control of gene expression in the mouse. Nat Rev Genet 2001; 2:743-55; PMID:11584291; http://dx.doi.org/10.1038/35093537
  • Sauer B, Henderson N. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc Natl Acad Sci USA 1988; 85:5166-70; PMID:2839833; http://dx.doi.org/10.1073/pnas.85.14.5166
  • Sternberg N, Hamilton D, Hoess R. Bacteriophage P1 site-specific recombination: II. Recombination between loxP and the bacterial chromosome. J Mol Biol 1981; 150:487-507; PMID:6276558; http://dx.doi.org/10.1016/0022-2836(81)90376-4
  • Nagy A. Cre recombinase: The universal reagent for genome tailoring. Genesis 2000; 26:99-109; PMID:10686599; http://dx.doi.org/10.1002/(SICI)1526-968X(200002)26:2%3c99::AID-GENE1%3e3.0.CO;2-B
  • Araki K, Imaizumi T, Okuyama K, Oike Y, Yamamura K-I. Efficiency of Recombination by Cre Transient Expression in Embryonic Stem Cells: Comparison of Various Promoters. J Biochem 1997; 122:977-82; PMID:9443813; http://dx.doi.org/10.1093/oxfordjournals.jbchem.a021860
  • Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 1999; 23:99-103; PMID:10471508; http://dx.doi.org/10.1038/12703
  • Coppari R, Ichinose M, Lee CE, Pullen AE, Kenny CD, McGovern RA, Tang V, Liu SM, Ludwig T. The hypothalamic arcuate nucleus: A key site for mediating leptin's effects on glucose homeostasis and locomotor activity. Cell Metabolism 2005; 1:63-72; PMID:16054045; http://dx.doi.org/10.1016/j.cmet.2004.12.004
  • Lazarus M, Shen H-Y, Cherasse Y, Qu W-M, Huang Z-L, Bass CE, Winsky-Sommerer R, Semba K, Fredholm BB, Boison D, et al. Arousal Effect of Caffeine Depends on Adenosine A2A Receptors in the Shell of the Nucleus Accumbens. J Neurosci 2011; 31:10067-75; PMID:21734299; http://dx.doi.org/10.1523/JNEUROSCI.6730-10.2011
  • Anaclet C, Lin J-S, Vetrivelan R, Krenzer M, Vong L, Fuller PM, Lu J. Identification and Characterization of a Sleep-Active Cell Group in the Rostral Medullary Brainstem. J Neurosci 2012; 32:17970-6; PMID:23238713; http://dx.doi.org/10.1523/JNEUROSCI.0620-12.2012
  • Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998; 391:806-11; PMID:9486653; http://dx.doi.org/10.1038/35888
  • Mochizuki T, Arrigoni E, Marcus JN, Clark EL, Yamamoto M, Honer M, Borroni E, Lowell BB, Elmquist JK, Scammell TE. Orexin receptor 2 expression in the posterior hypothalamus rescues sleepiness in narcoleptic mice. Proc Natl Acad Sci USA 2011; 108:4471-6; PMID:21368172; http://dx.doi.org/10.1073/pnas.1012456108
  • Gautron L, Lazarus M, Scott MM, Saper CB, Elmquist JK. Identifying the efferent projections of leptin-responsive neurons in the dorsomedial hypothalamus using a novel conditional tracing approach. J Comp Neurol 2010; 518:2090-108; PMID:20394060; http://dx.doi.org/10.1002/cne.22323
  • Zhang J, Xu Q, Yuan X, ChÈrasse Y, Schiffmann SN, De Kerchove D'ExaErde A, Qu W, Urade Y, Lazarus M, Huang Z, et al. Projections of nucleus accumbens adenosine A2A receptor neurons in the mouse brain and their implications in mediating sleep-wake regulation. Front Neuroanat 2013; 7(43):1-15; PMID: 24409122; http://dx.doi.org/10.3389/fnana.2013.00043 Front Neuroanat. 2013 Dec 10;7:43. doi: 10.3389/fnana.2013.00043. eCollection 2013. PubMed PMID: 24409122; PubMed Central PMCID: PMC3857888.
  • Deisseroth K, Feng G, Majewska AK, Miesenböck G, Ting A, Schnitzer MJ. Next-Generation Optical Technologies for Illuminating Genetically Targeted Brain Circuits. J Neurosci 2006; 26:10380-6; PMID:17035522; http://dx.doi.org/10.1523/JNEUROSCI.3863-06.2006
  • Pastrana E. Optogenetics: controlling cell function with light. Nat Meth 2011; 8:24-5; http://dx.doi.org/10.1038/nmeth.f.323
  • Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature 2007; 450:420-4; PMID:17943086; http://dx.doi.org/10.1038/nature06310
  • Tsunematsu T, Kilduff TS, Boyden ES, Takahashi S, Tominaga M, Yamanaka A. Acute Optogenetic Silencing of Orexin/Hypocretin Neurons Induces Slow-Wave Sleep in Mice. J Neurosci 2011; 31:10529-39; PMID:21775598; http://dx.doi.org/10.1523/JNEUROSCI.0784-11.2011
  • Williams RH, Chee MJS, Kroeger D, Ferrari LL, Maratos-Flier E, Scammell TE, Arrigoni E. Optogenetic-Mediated Release of Histamine Reveals Distal and Autoregulatory Mechanisms for Controlling Arousal. J Neurosci 2014; 34:6023-9; PMID:24760861; http://dx.doi.org/10.1523/JNEUROSCI.4838-13.2014
  • Anaclet C, Ferrari L, Arrigoni E, Bass CE, Saper CB, Lu J, Fuller PM. The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nat Neurosci 2014; 17:1217-24; PMID:25129078; http://dx.doi.org/10.1038/nn.3789
  • Zamir N, Skofitsch G, Bannon MJ, Jacobowitz DM. Melanin-concentrating hormone: unique peptide neuronal system in the rat brain and pituitary gland. Proc Natl Acad Sci USA 1986; 83:1528-31; PMID:3513180; http://dx.doi.org/10.1073/pnas.83.5.1528
  • Jego S, Glasgow SD, Herrera CG, Ekstrand M, Reed SJ, Boyce R, Friedman J, Burdakov D, Adamantidis AR. Optogenetic identification of a rapid eye movement sleep modulatory circuit in the hypothalamus. Nat Neurosci 2013; 16:1637-43; PMID:24056699; http://dx.doi.org/10.1038/nn.3522
  • Konadhode RR, Pelluru D, Blanco-Centurion C, Zayachkivsky A, Liu M, Uhde T, Glen WB, van den Pol AN, Mulholland PJ, Shiromani PJ. Optogenetic Stimulation of MCH Neurons Increases Sleep. J Neurosci 2013; 33:10257-63; PMID:23785141; http://dx.doi.org/10.1523/JNEUROSCI.1225-13.2013
  • Tsunematsu T, Ueno T, Tabuchi S, Inutsuka A, Tanaka KF, Hasuwa H, Kilduff TS, Terao A, Yamanaka A. Optogenetic Manipulation of Activity and Temporally Controlled Cell-Specific Ablation Reveal a Role for MCH Neurons in Sleep/Wake Regulation. J Neurosci 2014; 34:6896-909; PMID:24828644; http://dx.doi.org/10.1523/JNEUROSCI.5344-13.2014
  • Sprengel R, Hasan MT. Tetracycline-controlled genetic switches. Handb Exp Pharmacol 2007; 178:49-72; PMID:17203651; http://dx.doi.org/10.1007/978-3-540-35109-2_3
  • Tanaka KF, Matsui K, Sasaki T, Sano H, Sugio S, Fan K, Hen R, Nakai J, Yanagawa Y, Hasuwa H, et al. Expanding the repertoire of optogenetically targeted cells with an enhanced gene expression system. Cell Rep 2012; 2:397-406; PMID:22854021; http://dx.doi.org/10.1016/j.celrep.2012.06.011
  • Tsunematsu T, Tabuchi S, Tanaka KF, Boyden ES, Tominaga M, Yamanaka A. Long-lasting silencing of orexin/hypocretin neurons using archaerhodopsin induces slow-wave sleep in mice. Behav Brain Res 2013; 255:64-74; PMID:23707248; http://dx.doi.org/10.1016/j.bbr.2013.05.021
  • Lerchner W, Xiao C, Nashmi R, Slimko EM, van Trigt L, Lester HA, Anderson David J. Reversible Silencing of Neuronal Excitability in Behaving Mice by a Genetically Targeted, Ivermectin-Gated Cl− Channel. Neuron 2007; 54:35-49; PMID:17408576; http://dx.doi.org/10.1016/j.neuron.2007.02.030
  • Oishi Y, Williams RH, Agostinelli L, Arrigoni E, Fuller PM, Mochizuki T, Saper CB, Scammell TE. Role of the Medial Prefrontal Cortex in Cataplexy. J Neurosci 2013; 33:9743-51; PMID:23739971; http://dx.doi.org/10.1523/JNEUROSCI.0499-13.2013
  • Rogan SC, Roth BL. Remote Control of Neuronal Signaling. Pharmacol Rev 2011; 63:291-315; PMID:21415127; http://dx.doi.org/10.1124/pr.110.003020
  • Dong S, Allen JA, Farrell M, Roth BL. A chemical-genetic approach for precise spatio-temporal control of cellular signaling. Mol Bio Systems 2010; 6:1376-80
  • Alexander GM, Rogan SC, Abbas AI, Armbruster BN, Pei Y, Allen JA, Nonneman RJ, Hartmann J, Moy SS, Nicolelis MA, et al. Remote Control of Neuronal Activity in Transgenic Mice Expressing Evolved G Protein-Coupled Receptors. Neuron 2009; 63:27-39; PMID:19607790; http://dx.doi.org/10.1016/j.neuron.2009.06.014
  • Nawaratne V, Leach K, Suratman N, Loiacono RE, Felder CC, Armbruster BN, Roth BL, Sexton PM, Christopoulos A. New insights into the function of M4 muscarinic acetylcholine receptors gained using a novel allosteric modulator and a DREADD (Designer Receptor Exclusively Activated by a Designer Drug). Mol Pharmacol 2008; 74:1119-31; PMID:18628403; http://dx.doi.org/10.1124/mol.108.049353
  • Sasaki K, Suzuki M, Mieda M, Tsujino N, Roth B, Sakurai T. Pharmacogenetic Modulation of Orexin Neurons Alters Sleep/Wakefulness States in Mice. PLoS ONE 2011; 6:e20360; PMID:21647372; http://dx.doi.org/10.1371/journal.pone.0020360
  • Inutsuka A, Inui A, Tabuchi S, Tsunematsu T, Lazarus M, Yamanaka A. Concurrent and robust regulation of feeding behaviors and metabolism by orexin neurons. Neuropharmacol 2014; 85:451-60; http://dx.doi.org/10.1016/j.neuropharm.2014.06.015
  • Vardy E, Robinson JE, Li C, Olsen Reid HJ, DiBerto Jeffrey F, Giguere Patrick M, Sassano Flori M, Huang X-P, Zhu H, Urban Daniel J, et al. A New DREADD Facilitates the Multiplexed Chemogenetic Interrogation of Behavior. Neuron 2015; 86:936-46; PMID:25937170; http://dx.doi.org/10.1016/j.neuron.2015.03.065
  • Sakaguchi M, Kim K, Yu LMY, Hashikawa Y, Sekine Y, Okumura Y, Kawano M, Hayashi M, Kumar D, Boyden ES, et al. Inhibiting the Activity of CA1 Hippocampal Neurons Prevents the Recall of Contextual Fear Memory in Inducible ArchT Transgenic Mice. PLoS ONE 2015; 10:e0130163; PMID:26075894; http://dx.doi.org/10.1371/journal.pone.0130163
  • Goto A, Nakahara I, Yamaguchi T, Kamioka Y, Sumiyama K, Matsuda M, Nakanishi S, Funabiki K. Circuit-dependent striatal PKA and ERK signaling underlies rapid behavioral shift in mating reaction of male mice. Proc Natl Acad Sci USA 2015; 112:6718-23; PMID:25964359; http://dx.doi.org/10.1073/pnas.1507121112
  • Sweeney ST, Broadie K, Keane J, Niemann H, O'Kane CJ. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 1995; 14:341-51; PMID:7857643; http://dx.doi.org/10.1016/0896-6273(95)90290-2
  • Hikida T, Kimura K, Wada N, Funabiki K, Nakanishi S. Distinct Roles of Synaptic Transmission in Direct and Indirect Striatal Pathways to Reward and Aversive Behavior. Neuron 2010; 66:896-907; PMID:20620875; http://dx.doi.org/10.1016/j.neuron.2010.05.011
  • Garner AR, Rowland DC, Hwang SY, Baumgaertel K, Roth BL, Kentros C, Mayford M. Generation of a Synthetic Memory Trace. Science 2012; 335:1513-6; PMID:22442487; http://dx.doi.org/10.1126/science.1214985
  • Ramirez S, Liu X, Lin P-A, Suh J, Pignatelli M, Redondo RL, Ryan TJ, Tonegawa S. Creating a False Memory in the Hippocampus. Science 2013; 341:387-91; PMID:23888038; http://dx.doi.org/10.1126/science.1239073
  • Liu X, Ramirez S, Pang PT, Puryear CB, Govindarajan A, Deisseroth K, Tonegawa S. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 2012; 484:381-5; PMID:22441246; http://dx.doi.org/10.1038/484410a
  • Zhang Z, Ferretti V, Guntan I, Moro A, Steinberg EA, Ye Z, Zecharia AY, Yu X, Vyssotski AL, Brickley SG, et al. Neuronal ensembles sufficient for recovery sleep and the sedative actions of ; alpha2 adrenergic agonists. Nat Neurosci 2015; 18:553-61; PMID:25706476; http://dx.doi.org/10.1038/nn.3957
  • Callaway EM. A molecular and genetic arsenal for systems neuroscience. Trends Neurosci 2005; 28:196-201; PMID:15808354; http://dx.doi.org/10.1016/j.tins.2005.01.007
  • Huang Z-L, Urade Y, Hayaishi O. Prostaglandins and adenosine in the regulation of sleep and wakefulness. Curr Opin Pharmacol 2007; 7:33-8; PMID:17129762; http://dx.doi.org/10.1016/j.coph.2006.09.004
  • Huang ZL, Urade Y, Hayaishi O. The role of adenosine in the regulation of sleep. Curr Top Med Chem 2011; 11:1047-57; PMID:21401496; http://dx.doi.org/10.2174/156802611795347654
  • Lazarus M, Huang Z-L, Lu J, Urade Y, Chen J-F. How do the basal ganglia regulate sleep–wake behavior? Trends Neurosci 2012; 35:723-32; PMID:22858523; http://dx.doi.org/10.1016/j.tins.2012.07.001
  • 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 2013; 23:780-5; PMID:23465424; http://dx.doi.org/10.1016/j.conb.2013.02.001
  • Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci USA 2003; 100:13940-5; PMID:14615590; http://dx.doi.org/10.1073/pnas.1936192100
  • Bamann C, Kirsch T, Nagel G, Bamberg E. Spectral Characteristics of the Photocycle of Channelrhodopsin-2 and Its Implication for Channel Function. J Mol Biol 2008; 375:686-94; PMID:18037436; http://dx.doi.org/10.1016/j.jmb.2007.10.072