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Laterality
Asymmetries of Brain, Behaviour, and Cognition
Volume 26, 2021 - Issue 1-2: Laterality in animals
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Original Papers

Adaptation and survival: hypotheses about the neural mechanisms of unihemispheric sleep

Pages 71-93 | Received 11 May 2020, Accepted 19 Sep 2020, Published online: 14 Oct 2020

References

  • Adamantidis, A. R., Zhang, F., Aravanis, A. M., Deisseroth, K., & de Lecea, L. (2007). Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature, 450, 420–424.
  • Allada, R., & Siegel, J. M. (2008). Unearthing the phylogenetic roots of sleep. Current Biology, 18, R670–R679.
  • Anaclet, C., Ferrari, L., Arrigoni, E., Bass, C. E., Saper, C. B., Lu, J., … Fuller, P. M. (2014). The GABAergic parafacial zone in a medullary slow wave sleep-promoting center. Nature Neuroscience, 17, 1217–1224.
  • Anaclet, C., Pedersen, N. P., Ferrari, L. L., Venner, A., Bass, C. E., Arrigoni, E., … Fuller, P. M. (2015). Basal forebrain control of wakefulness and cortical rhythms. Nature Communications, 6, 8744.
  • Andretic, R., van Swinderen, B., & Greespan, R. J. (2005). Dopaminergic modulation of arousal in Drosophila. Current Biology, 15, 1165–1175.
  • Barlow, I. L., & Rihel, J. (2017). Zebrafish sleep: From geneZZZ to neuronZZZ. Current Opinion in Neurobiology, 44, 65–71.
  • Berlucchi, G. (1966). Electroencephalographic studies in split brain cats. Electroencephalography and Clinical Neurophysiology, 20, 348–356.
  • Blakely, R. D., & Edwards, R. H. (2012). Vesicular and plasma membrane transporters for neurotransmitters. Cold Sping Harbour Prospects in Biology, 4, a005595.
  • Blanco-Centurion, C., Garashchenko, D., & Shiromani, P. J. (2007). Effects of saporin-induced lesions of three arousal populations on daily levels of sleep and wake. Journal of Neuroscience, 27, 14041–14048.
  • Bobbo, D., Galvani, F., Mascetti, G. G., & Vallortigara, G. (2002). Light exposure of chick embryo influences monocular sleep. Behavioral Brain Research, 134, 447–466.
  • Bonnavion, P., & de Lecea, L. (2010). Hypocretins in the control of sleep and wakefulness. Current Neurology and Neuroscience Reports, 10, 174–179.
  • Borbely, A. (1982). A two process model of sleep regulation. Human Neurobiology, 1, 195–204.
  • Borbely, A., Daan, S., Wirz-Justice, A., & Deboer, T. (2016). The two process model of sleep regulation. A reappraisal. Journal of Sleep Research, 25, 131–143.
  • Boucetta, S., Cisse, Y., Mainville, L., Morales, M., & Jones, B. E. (2014). Discharge profiles across the sleep-waking cycle of identified cholinergic GABAergic and glutamatergic neurons in the pontomesencephalic tegmentum in the rat. Journal of Neuroscience, 34, 4708–4727.
  • Cespuglio, R., Amroumi, D., Meiller, A., Buguet, A., & Gautier-Sauvigné, S. (2012). Nitric oxide in the regulation of the sleep-wake states. Sleep Medicine Reviews, 16, 265–279.
  • Chemelli, R. M., Willie, J. T., Sinton, C. M., Elmquist, J. K., Scammell, T. E., Lee, C., … Saper, C. B. (1999). Narcolepsy in orexin knockout mice: Molecular genetics of sleep regulation. Cell, 98, 437–451.
  • Chou, T. C., Scammell, T. E., Gooley, J. J., Gauss, S. E., Saper, C. B., & Lu, J. (2003). Critical role of dorsomedial hypothalamic nucleus in a wide range of behavioral circadian rhythms. The Journal of Neuroscience, 23, 10691–10702.
  • Colwell, C. S. (2011). Linking neural activity and molecular oscillations in the SCN. Nature Review of Neuroscience, 12, 553–569.
  • Dell, L.-A., Karlsson, K. A. E., Patzke, N., Spocter, M. A., Siegel, J. M., & Manger, P. R. (2016). Organization of the sleep-related neural systems in the brain of the Minke-Wale (Balaenoptera acutorostrata). The Journal of Comparative Neurology, 524, 2018–2035.
  • Dell, L.-A., Patzke, N., Bhagwandin, A., Bux, F., Fuxe, K., Barber, G., … Manger, P. R. (2012). Organization and number of orexinergic neurons in the hypothalamus of two species of Cetartiodactyla: A comparison of giraffe (Giraffa camelopardalis) and harbour porpoise (Phocoema phocoema). Journal of Chemical Neuroanatomy, 44, 98–109.
  • Dell, L.-A., Patzke, N., Spocter, M. A., Bertelsen, M. F., Siegel, J. M., & Manger, P. R. (2016). Organization of the sleep-related neural systems in the brain of the River Hippopotamus (Hippopotamus amphibius): A most unusual Cetartiodactil species. The Journal of Comparative Neurology, 524, 2036–2058.
  • Dell, L.-A., Patzke, N., Spocter, M. A., Siegel, J. M., & Manger, P. R. (2016). Organization of sleep-related neural systems in the brain of the harbour porpoise (Phocoema phocoema). The Journal of Comparative Neurology, 524, 1999–2017.
  • Eban-Rothschild, A., Appelbaum, L., & de Lecea, L. (2018). Neuronal mechanisms for sleep/wake regulation and modulatory drive. Neuropsychopharmacology, 43, 937–952.
  • Fuchs, T., Haney, A., Jechura, J., Moore, F. R., & Bingman, V. P. (2006). Daytime naps in night-migrating birds: Behavioral adaptation to seasonal sleep deprivation in the Swainson thrush (Catharus ustulatus). Animal Behavior, 72, 951–958.
  • Fuller, P. M., Gooley, J. J., & Saper, C. B. (2006). Neurobiology of sleep-wake cycle, sleep architecture, circadian regulation and regulatory feedback. Sleep, 21, 482–493.
  • Fuller, P. M., Sherman, D., Pedersen, N. P., Saper, C. B., & Lu, J. (2011). Reassessment of the structural basis of the ascending arousal system. The Journal of Comparative Neurology, 519, 933–956.
  • Gaston, K. E., & Gaston, M. G. (1984). Unilateral memory after binocular discrimination training: Left hemisphere dominance in chicks? Brain Research, 303, 190–193.
  • Gerashchenko, D., Wisor, J. P., Burns, D., Reh, R. K., Shiromani, P. J., Sakurai, T., … Kilduff, T. S. (2008). Identification of a population of sleep-active cerebral cortex neurons. Proceedings of the National Academy of Sciences, 105, 10227–10232.
  • Halassa, M. M., Florian, C., Fellin, T., Munoz, J. R., Lee, S. Y., Abel, T., … Frank, M. G. (2009). Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss. Neuron, 61, 213–219.
  • Hassani, O. K., Lee, M. G., Henry, P., & Jones, B. E. (2009). Discharge profiles of identified GABAergic in comparison to cholinergic and putative glutamatergic basal forebrain neurons across the sleep-wake cycle. Journal of Neuroscience, 29, 11828–11840.
  • Herrera, C. G., Cadavieco, M. C., Jego, S., Ponimarenko, A., Korotkova, T., & Adamantidis, A. (2016). Hypothalamic feedforward inhibition of thalamocortical network controls arousal and consciousness. Nature Neuroscience, 19, 290–298.
  • Hobson, J. A. (2005). Sleep is of the brain, by the brain and for the brain. Insight commentary. Nature, 437, 1254–1256. doi:10.1038/nature04283
  • Huelsmann, M., Hecker, N., Springer, M. S., Gatesy, J., Shama, V., & Hiller, M. (2019). Genes lost during the transition from land to water in cetaceans highlight genomic changes associated with aquatic adaptations. Science Advances, 5, eaaw6671.
  • Irmark, S. O., & de Lecea, L. (2014). Basal forebrain cholinergic modulation of sleep transitions. Sleep, 37, 1941–1951.
  • Joiner, W. J. (2016). Unrevealing the evolutionary determinants of sleep. Current Biology, 26, R1073–R1087.
  • Kaur, S., Pedersen, N. P., Yokota, S., Hur, E. E., Fuller, P. M., Lazarus, M., … Saper, C. B. (2013). Glutamatergic signaling from the parabrachial nucleus plays a critical role in hypercapnic arousal. Journal of Neuroscience, 33, 7627–7640.
  • Kedziora, D. I., Abeysuriya, P. G., Phillips, A. J. K., & Robinson, P. A. (2012). Physiologically based quantitative modeling of unihemispheric sleep. Journal of Theoretical Biology, 314, 109–119.
  • Kim, T., Thankachan, S., Mckenna, J.T., McNally, J. M., Yang, C. Choi, J. M., … McCarley, R. W. (2015). Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations. Proceedings of the National Academy of Science, USA, 112, 3535–3540.
  • Kim, C. K., Adhikari, A., & Deisseroth, K. (2017). Integration of optogenetics with complementary methodologies in systems neuroscience. Nature Reviews of Neuroscience, 18, 222–235.
  • Kovach, J. K. J. (1968). Spatial orientation of chick embryo during the last five days of incubation. Journal of Comparative and Physiological Psychology, 66, 283–288.
  • Kovalzon, V. M. (1977). Brain temperature variations and ECoG in free swimming bottlenose dolphin. In P. W. P. Koella Levin & W. P. Levin (Eds.), Sleep. Third European sleep Research Congress (pp. 239–241). Montpellier, Basel: Karger.
  • Kovalzon, V. M., & Mukhametov, L. M. (1982). Temperature variations in the brain corrisponding to unihemispheric slow wave sleep in dolphins. Journal of Evolutionary Biochemestry and Physiology, 18, 307–309.
  • Kroeger, J. M., Clinton, J. M., Winters, B. D., Zielinski, M. R., Taishi, P., Jewett, K. A., … Davis, C. J. (2011). Involvement of cytokines in slow wave sleep. Progress in BrainResearch, 193, 39–47.
  • Kroeger, D., Ferrari, L. L., Arrigoni, E., Scammell, T. E., Saper, C. B., & Vetrilevan, R. (2016). Optogenetic activation of VLPO galaninergic neurons promotes sleep in mice. Society of Neuroscience Abstacts, 41, 816. 13. Cited by Saper C.B. (2016).
  • Kroeger, D., Ferrari, L. L., Petit, G., Mahoney, G. E., Fuller, P. M., Arrigoni, E., … Scammell, T. E. (2017). Cholinergic, glutamatergic and GABAergic neurons of the pedunculopontine tegmental nucleus have distinct effects on sleep/wake behavior in mice. The Journal of Neuroscience, 37, 1352–1366.
  • Kume, K., Kume, S., Park, S. K., Hirsh J., & Jackson, F. R. (2005). Dopamine is a regulator of arousal in the fruit fly. Journal of Neuroscience, 25, 7377–7384.
  • Lapierre, J. L., Kosenko, P. O., Lyamin, O. I., Kodama, T., Mukhametov, L. M., & Siegel, J. M. (2007). Cortical acetylcholine release is lateralized during asymmetrical slow-wave sleep in northern Fur seals. Journal of Neuroscience, 27, 11999–12006.
  • Lee, M. G., Hassani, O. K., & Jones, B. E. (2005). Discharge of identified orexin/hypocretin neurons across the sleep-waking cycle. Journal of Neuroscience, 25, 6716–6720.
  • Lesku, J. A., Rattenborg, N. C., Valcu, M., Vyssotsky, A. L., Kuhn, S., Kuemmeth, F., … Kempenaers, B. (2012). Adaptative sleep loss in polygynous pectoral sandpipers. Science, 337, 1654–1658.
  • Levitas-Djerby, T., & Appelbaum, L. (2017). Modeling sleep and neuropsychiatrc disorders in zebrafish. Current Opinion in Neurobiology, 44, 89–93.
  • Lin, M. Z., & Schnitzer, M. J. (2016). Genetically encoded indicators of neural activity. Nature Neuroscience, 19, 1142–1153.
  • Luppi, P.-H., Peyron, C., & Fort, P. (2017). Not a single but multiple populations of GABAergic neurons control sleep. Sleep Medicine Reviews, 32, 85–94.
  • Lyamin, O. I., Lapierre, J. L., Kosenko, P. O., Kodama, T., Bhagwandin, A., Korneva, S. M., … Siegel, J. M. (2016). Monoamine release during unihemispheric sleep and unihemispheric waking in the fur seal. Sleep, 39, 625–636.
  • Lyamin, O. I., Manger, P. R., Ridgway, S. A., Mukhametov, L. M., & Siegel, J. M. (2008). Cetacean sleep: An unusual form of mammalian sleep. Neuroscience and Biobehavioral Review, 32, 1451–1484.
  • Lyamin, O. I., & Mukhametov, L. M. (2017). Sleep in the northern fur seal. Current Opinion in Neurobiology, 44, 144–151.
  • Manger, P. R., Ridgway, S. H., & Siegel, J. M. (2003). The locus coeruleus of bottlenose dolphin (Tursioupus truncatus) as revealed by tyrosine hydroxylase immunehistochemestry. Journal of Sleep Research, 12, 149–155.
  • Mascetti, G. G. (2016). Unihemispheric sleep and asymmetrical sleep: Behavioral, neurophysiological, and functional perspectives. Nature and Science of Sleep, 8, 221–238.
  • Mascetti, G. G., Rugger, M., Vallortigara, G., & Bobbo, D. (2006). Monocular- unihemispheric sleep and visual discrimination learning in the domestic chick. Experimental Brain Research, 176, 70–84.
  • Mascetti, G. G., & Vallortigara, G. (2001). Why birds sleep with one eye open? Light exposure of chick embryo as a determinant of monocular sleep. Current Biology, 11, 971–974.
  • McGinty, D., & Szymusiak, R. (1990). Keeping cool: An hypothesis about the mechanisms and functions of slow wave sleep. Trends in Neurosciences, 13, 480–487.
  • Michel, M., & Lyons, L. C. (2014). Unraveling the complexities of circadian and sleep interactions with memory formation through invertebrate research. Frontiers in System Neuroscience, 8, 133.
  • Michel, F., & Roffwarg, H. P. (1967). Chronic split brain stem preparation: Effect on the sleep-waking cycle. Experientia, 23, 126–128.
  • Montplaisir, J., Nielsen, T., Cote, J., Boivin, D., Rouleau, I., & Lapierre, G. (1990). Interhemispheric EEG coherence before and after partial callosotomy. Clinical Electroencephalography, 21, 42–47.
  • Morairty, S. R., Dittrich, L., Pasumarhi, R. K., Valladao, D., Heiss, J. E., Garashchenko, D., … Kilduff, T. S. (2013). A role for cortical nNOS/NK1 neurons in coupling homeostatic sleep drive to EEG slow wave activity. Proceedings of the National Academy of Sciences, 110, 20272–20277.
  • Moruzzi, G., & Magoun, H. V. (1949). Brain stem reticular formation and activation of the EEG. Electroencephalography and Clinical Neurophysiology, 1, 455–473.
  • Mukhametov, L. M. (1987). Unihemispheric slow wave sleep in the Amazonian dolphin, Inia geoffrensis. Neuroscience Letters, 79, 128–132.
  • Mukhametov, L. M. (1988). The absence of paradoxical sleepin dolphins. In W. P. Koella, L. F. Oba, H. Schulz, & P. Visser (Eds.), Sleep `86 (pp. 154–156). Stuttgart: Gustav Spinger Verlag.
  • Mukhametov, L. M., Lyamin, O. I., & Polyakova, I. G. (1985). Interhemispheric asynchrony of the sleep EEG in northern fur seals. Experientia, 41, 1034–1035.
  • Mukhametov, L. M., Oleksenko, A. I., & Polyakova, I. G. (1988). Quantitative chararacteristics of the electroencepalographic sleep stages in bottlenose dolphins. Neurophisioloziya, 20, 532–538.
  • Mukhametov, L. M., Supin, A. Y., & Polyakova, I. G. (1977). Interhemispheric asymmetry of the electroncephalographic sleep pattern in dolphins. Brain Research, 134, 581–584.
  • Nall, A., & Sehgal, A. (2014). Monoamines and sleep in Drosophila. Behavioral Neuroscience, 128, 264–272.
  • Nelini, C., Bobbo, D., & Mascetti, G. G. (2010). Local sleep: Spatial learning task enhances sleep in the right hemisphere of domestic chics (gallus gallus). Experimental Brain Research, 205, 195–204.
  • Nelini, C., Bobbo, D., & Mascetti, G. G. (2012). Monocular learning of a spatial task enhances sleep in the right hemisphere of domestic chick (gallus gallus). Experimental Brain Research, 218, 381–388.
  • Nielsen, T., Montplaisir, J., & Lassonde, M. (1993). Decrease interhemispheric coherence during sleep in agenesis of corpus callosum. European Neurology, 33, 173–176.
  • Ookawa, T., & Gotoh, J. (1964). Electroencephalographic study of chickens: Periodic recurrence of low voltage and fast waves during behavioral sleep. Poultry Science, 43, 1603–1604.
  • Ookawa, T., & Takagi, K. (1968). Electroencephalograms of free behavioral chicks at various developmental ages. Japanese Journal of Physiology, 18, 87–99.
  • Pedersen, N. P., Saper, C. B., & Fuller, P. M. (2016). Activation of Nos 1 neurons in the caudal hypothalamus produces prolonged wakefulness. Society of Neuroscience Abstracts, 42, 254–257. Cited by Saper C.B. & Fuller, P.M. (2016).
  • Phillips, A. J. K., & Robinson, P. A. (2007). A Quantitative model of sleep-wake dynamics based on the physiology of the brainstem ascending arousal system. Journal of Biological Rhythms, 22, 167–179.
  • Porkka-Heiskannen, T. (2013). Sleep homeostasis. Current Opinion in Neurobiology, 23, 799–805.
  • Porkka-Heiskannen, T., Strecker, R. E., Thakkar, M., Bjorkum, A. A., Greene, R. V., & McCarley, R. W. (1997). Adenosine: A mediator of the sleep-induced effects of prolonged wakefulness. Science, 276, 1265–1268.
  • Radulovaki, M., Virus, R. M., Djuricic-Nedelson, M., & Green, R. D. (1984). Adenosine analogs and sleep in rats. Journal of Pharmachology and Experimental Therapeutics, 228, 268–274.
  • Rattenborg, N. C., Amlaner, C. J., & Lima, S. L. (2000). Behavioral, neurophysiological and evolutionary perpectives of unihemispheric sleep. Neuroscience and Biobehavioral Review, 24, 817–842.
  • Rattenborg, N. C., Lima, S. L., & Amlaner, C. J. (1999a). Facultative control of avian unihemispheric sleep under the risk of predation. Behavioural Brain Research, 105, 163–172.
  • Rattenborg, N. C., Lima, S. L., & Amlaner, C. J. (1999b). Half awake to the risk of predation. Nature, 397, 397–398.
  • Rattenborg, N. C., Voirin, B., Cruz, S. M., Tisdale, R., Dell’Omo, G., Lipp, H. P., … Vyssolski, A. L. (2016). Evidence that birds sleep in mid-flight. Nature Communications, 7, 12468. doi:10.1038/ncomms12468
  • Rattenborg, N. G., van der Meij, J., Beckers, G. J. L., & Lesku, J. A. (2019). Local aspects of avian Non-REM and REM sleep. Frontiers in Neuroscience, 13, 1–16. doi:10.3389/fnins.2019.00567
  • Ridgway, S. H., Houser, D., Finneran, J., Carter, D., Keogh, M., Van Bonin, W., … Hoch, C. (2006). Functional imaging of dolphin brain metabolism and blood flow. Journal of Experimental Biology, 209, 2902–2910.
  • Rogers, L. J. (1982). Light experience and asymmetry of brain function. Nature, 297, 223–225.
  • Saper, C. B. (1985). Organization of cerebral cortical afferents systems in the rat II. Hypotalamocortical projections. The Journal of Comparative Neurology, 237, 21–46.
  • Saper, C. B., & Fuller, P. M. (2017). Wake-sleep circuitry: An overview. Current Opinions in Neurobiology, 44, 186–192.
  • Saper, C. B., Fuller, P. M., Pedersen, N. P., Lu, J., & Scammell, T. E. (2010). Sleep state switching. Neuron, 68, 1023–1042.
  • Sasaki, K., Suzuki, M., Mieda, M., Tsujino, N., Roth, B., & Sakurai, T. (2011). Pharmacogenetic modulation of orexin neurons alters sleep/wakefulness states in mice. Plos One, 6, e20360. Cited by Scarmmell, T.E. et al. (2017).
  • Scammell, T. E., Arrigoni, E., & Lipton, J. O. (2017). Neural circuitry of wakefulness and sleep. Neuron, 93, 747–765.
  • Schmitt, L. I., Sims, R. E., Dale, N., & Haydon, P. G. (2012). Wakefulness affects synaptic and network activity by increasing extracellular astrocyte-derived adenosine. Journal of Neuroscience, 32, 4417–4425.
  • Sherin, J. E., Elmquist, J. R., Torrealba, F., & Saper, C. B. (1998). Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. The Journal of Neuroscience, 18, 4705–4721.
  • Suntsova, N., Szymusiak, R., Alam, M. N., Guzman-Marin, R., & McGinty, D. (2002). Sleep-waking discharge patterns of medial preoptic nucleus neurons in rats. The Journal of Physiology, 543, 665–677.
  • Szymusiak, R., Steininger, T., Alam, N., & McGinty, D. (2001). Preoptic area sleep-regulating mechanisms. Archives Italiennes de Biologie, 139, 77–92.
  • Tapley, R. G., & Ridgway, S. H. (1994). Corpus callosum size in delphinid cetaceans. Brain, Behavior and Evolution, 44, 156–165.
  • Tong, Q., Ye, C., Jones, J. E., Elmquist, J. K., & Lowell, B. B. (2008). Synaptic release of GABA by AgRP neurons is required for normal regulation of energy balance. Nature Neuroscience, 11, 998–1000.
  • Tong, Q., Ye, C., McCrimmon, R. J., Dhillon, H., Choi, B., Kamer, M. D., … Lowell, B. B. (2007). Synaptic glutamate release by ventromedial hypothalamic neurons is part of the neurocircuitry that prevents hypoglicemia. Cell Metabolism, 5, 383–393.
  • Vallortigara, G., Regolin, L., Bortolomiol, G., & Tommasi, L. (1996). Lateral asymmetries in eye use due to preference during visual discrimination learning in chicks. Behavioral Brain Research, 74, 135–143.
  • Vallortigara, G., & Rogers, L. J. (2005). Survival with an asymmetrical brain: Advantages and disadvantages of cerebral lateralization. Behavioral Brain Sciences, 28, 575–589.
  • Vallortigara, G., Zanforlin, M., & Cailotto, M. (1988). Right-left asymmetry in position learning of male chicks. Behavioral Brain Research, 27, 189–191.
  • Venner, A., Anaclet, C., Broadhurst, R. Y., Saper, C. B., & Fuller, P. M. (2016). A novel population of wake-promoting GABAergic neurons in the ventral lateral hypothalamus. Current Biology, 26, 2137–2143.
  • Von Economo, C. (1930). Sleep as a problem of localization. The Journal of Nervous and Mental Disease, 71, 249–259.
  • Vujovic, N., Gooley, J. J., Jhou, T. C., & Saper, C. B. (2015). Projections from the subparaventricular zone define four channels of output from the circadian timing system. Journal of Comparative Neurology, 523, 2714–2737.
  • Welsh, D. K., Takahashi, J. S., & Kay, S. A. (2010). Suprachiasmatic nucleus: Cell autonomy and network properties. Annual Review of Physiology, 72, 551–577.
  • Wu, M. N., Koh, K., Yue, Z., Joiner, W. J., & Sehgal, A. (2008). A genetic screen for sleep and circadian mutants reveals mechanisms underlying regulation of sleep in Drosophila. Sleep, 31, 465–472.
  • Xu, M., Chung, S., Zhang, P., Ma, C., Chang, W.-C., Weissbourd, B., … Dan, Y. (2015). Basal forebrain circuit for sleep-wake control. Nature Neuroscience, 18, 1641–1647.
  • Yamashita, T., & Yamanaka, A. (2017). Lateral hypothalamic circuits for sleep-wake control. Current Opinions in Neurobiology, 44, 94–100.
  • Zant, J. C., Kim, T., Prokai, L., Szarka, S., McNally, J., McKenna, J. T., … Basheer, R. (2016). Cholinergic neurons of the basal forebrain promote wakefulness by actions on neighboring non-cholinergic neurons. An opto-dialisis study. The Journal of Neuroscience, 36, 2057–2067.

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