A neuronal hub binding sleep initiation and body cooling in response to a warm external stimulus
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Mammals, including humans, prepare for sleep by nesting and/or curling up, creating microclimates of skin warmth. To address whether external warmth induces sleep through defined circuitry, we used c-Fos-dependent activity tagging, which captures populations of activated cells and allows them to be reactivated to test their physiological role. External warming tagged two principal groups of neurons in the median preoptic (MnPO)/medial preoptic (MPO) hypothalamic area. GABA neurons located mainly in MPO produced non-rapid eye movement (NREM) sleep but no body temperature decrease. Nitrergic-glutamatergic neurons in MnPO-MPO induced both body cooling and NREM sleep. This circuitry explains how skin warming induces sleep and why the maximal rate of core body cooling positively correlates with sleep onset. Thus, the pathways that promote NREM sleep, reduced energy expenditure, and body cooling are inextricably linked, commanded by the same neurons. This implies that one function of NREM sleep is to lower brain temperature and/or conserve energy.
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Anesthetics may use temperature-sensing molecular targets such as K2P channels or mitochondrial targets to link reduced body temperature with decreased metabolism as in sleep.
“anesthetics may rely on molecular targets with intrinsic temperature sensing ability such as the K2P channels or mitochondrial targets in critical cellular populations to inextricably link reductions in body temperature with decreased metabolism as occurs with endogenous sleep [111].”
From The Biology of General Anesthesia from Paramecium to Primate (2019) · cites this paper as [111]
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Cites
Genome-wide atlas of gene expression in the adult mouse brain
Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572 · see citing works
Rapid, reversible activation of AgRP neurons drives feeding behavior in mice
Krashes, M. J., Koda, S., Ye, C., Rogan, S. C., Adams, A. C., Cusher, D. S., Maratos-Flier, E., Roth, B. L., & Lowell, B. B. (2011) · Journal of Clinical Investigation · doi:10.1172/jci46229 · Cited by 1,578 · see citing works
Dijk, D., & Czeisler, C. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-05-03526.1995 · Cited by 1,356 · see citing works
Leptin Action on GABAergic Neurons Prevents Obesity and Reduces Inhibitory Tone to POMC Neurons
Vong, L., Ye, C., Yang, Z., Choi, B. J., Chua, S. C., & Lowell, B. B. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.028 · Cited by 1,203 · see citing works
Clues to the functions of mammalian sleep
Siegel, J. M. (2005) · Nature · doi:10.1038/nature04285 · Cited by 1,040 · see citing works
Chemogenetics revealed: DREADD occupancy and activation via converted clozapine
Gomez, J. L., Bonaventura, J., Lesniak, W., Mathews, W. B., Sysa-Shah, P., Rodriguez, L. A., Ellis, R. J., Richie, C. T., Harvey, B. K., Dannals, R. F., et al. (2017) · Science · doi:10.1126/science.aan2475 · Cited by 980 · see citing works
Neural Circuitry of Wakefulness and Sleep
Scammell, T. E., Arrigoni, E., & Lipton, J. O. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.014 · Cited by 966 · see citing works
Localization of a Stable Neural Correlate of Associative Memory
Reijmers, L. G. J. E., Perkins, B. L., Matsuo, N., & Mayford, M. R. (2007) · Science · doi:10.1126/science.1143839 · Cited by 853 · see citing works
Regulation of Body Temperature by the Nervous System
Tan, C. L., & Knight, Z. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.022 · Cited by 798 · see citing works
Mild Perioperative Hypothermia
Sessler, D. I. (1997) · New England Journal of Medicine · doi:10.1056/nejm199706123362407 · Cited by 711 · see citing works
VTA dopaminergic neurons regulate ethologically relevant sleep-wake behaviors
Eban-Rothschild, A., Rothschild, G., Giardino, W. J., Jones, J. R., & de Lecea, L. (2016) · Nature Neuroscience · doi:10.1038/nn.4377 · Cited by 583 · see citing works
Temperature Regulation in Laboratory Rodents
Gordon, C. J. (1993) · Cambridge University Press eBooks · doi:10.1017/cbo9780511565595 · Cited by 515 · see citing works
A thermosensory pathway that controls body temperature
Nakamura, K., & Morrison, S. F. (2007) · Nature Neuroscience · doi:10.1038/nn2027 · Cited by 503 · see citing works
Warm-Sensitive Neurons that Control Body Temperature
Tan, C. L., Cooke, E. K., Leib, D. E., Lin, Y.-C., Daly, G. E., Zimmerman, C. A., & Knight, Z. A. (2016) · Cell · doi:10.1016/j.cell.2016.08.028 · Cited by 402 · see citing works
Warm feet promote the rapid onset of sleep
Kräuchi, K., Cajochen, C., Werth, E., & Wirz-Justice, A. (1999) · Nature · doi:10.1038/43366 · Cited by 398 · see citing works
Natural Sleep and Its Seasonal Variations in Three Pre-industrial Societies
Yetish, G., Kaplan, H., Gurven, M., Wood, B., Pontzer, H., Manger, P. R., Wilson, C., McGregor, R., & Siegel, J. M. (2015) · Current Biology · doi:10.1016/j.cub.2015.09.046 · Cited by 395 · see citing works
The TRPM2 channel is a hypothalamic heat sensor that limits fever and can drive hypothermia
Song, K., Wang, H., Kamm, G. B., Pohle, J., Reis, F. D. C., Heppenstall, P. A., Wende, H., & Siemens, J. (2016) · Science · doi:10.1126/science.aaf7537 · Cited by 393 · see citing works
Keeping cool: a hypothesis about the mechanisms and functions of slow-wave sleep
McGinty, D., & Szymusiak, R. S. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90081-k · Cited by 390 · see citing works
Circuit-based interrogation of sleep control
Weber, F., & Dan, Y. (2016) · Nature · doi:10.1038/nature19773 · Cited by 378 · see citing works
A hypothalamic circuit that controls body temperature
Zhao, Z., Yang, W. Z., Gao, C., Fu, X., Zhang, W., Zhou, Q., Chen, W., Ni, X., Lin, J.-K., Yang, J., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616255114 · Cited by 352 · see citing works
VanSomeren, E. J. W. (2000) · Chronobiology International · doi:10.1081/cbi-100101050 · Cited by 329 · see citing works
Identification of preoptic sleep neurons using retrograde labelling and gene profiling
Chung, S., Weber, F., Zhong, P., Tan, C. L., Nguyen, T. N., Beier, K. T., Hörmann, N., Chang, W.-C., Zhang, Z., Do, J. P., et al. (2017) · Nature · doi:10.1038/nature22350 · Cited by 317 · see citing works
The effects of high and low ambient temperatures on human sleep stages
Haskell, E. H., Palca, J. W., Walker, J. M., Berger, R. J., & Heller, H. C. (1981) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(81)90226-1 · Cited by 302 · see citing works
The TRPM2 ion channel is required for sensitivity to warmth
Tan, C., & McNaughton, P. A. (2016) · Nature · doi:10.1038/nature19074 · Cited by 299 · see citing works
Schmidt, M. H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.08.001 · Cited by 291 · see citing works
Neural circuitry engaged by prostaglandins during the sickness syndrome
Saper, C. B., Romanovsky, A. A., & Scammell, T. E. (2012) · Nature Neuroscience · doi:10.1038/nn.3159 · Cited by 285 · see citing works
Neuronal ensembles sufficient for recovery sleep and the sedative actions of α2 adrenergic agonists
Zhang, Z., Ferretti, V., Güntan, İ., Moro, A., Steinberg, E. A., Ye, Z., Zecharia, A. Y., Yu, X., Vyssotski, A. L., Brickley, S. G., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3957 · Cited by 275 · see citing works
Self-citationA thermosensory pathway mediating heat-defense responses
Nakamura, K., & Morrison, S. F. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913358107 · Cited by 267 · see citing works
Wei, Y., Wang, S.-R., Jiao, Z., Zhang, W., Lin, J.-K., Li, X., Li, S., Zhang, X., & Xu, X. (2018) · Nature Communications · doi:10.1038/s41467-017-02648-0 · Cited by 253 · see citing works
Skin deep: enhanced sleep depth by cutaneous temperature manipulation
Raymann, R. J. E. M., Swaab, D. F., & Van Someren, E. J. W. (2008) · Brain · doi:10.1093/brain/awm315 · Cited by 218 · see citing works
Mechanisms and functions of coupling between sleep and temperature rhythms
Van Someren, E. J. W. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)53018-3 · Cited by 209 · see citing works
Szymusiak, R. S., Gvilia, I., & McGinty, D. (2007) · Sleep Medicine · doi:10.1016/j.sleep.2007.03.013 · Cited by 200 · see citing works
Leshan, R. L., Greenwald-Yarnell, M. L., Patterson, C. M., Gonzalez, I. E., & Myers, M. G. (2012) · Nature Medicine · doi:10.1038/nm.2724 · Cited by 163 · see citing works
Yu, S., Qualls‐Creekmore, E., Rezai-Zadeh, K. P., Jiang, Y., Berthoud, H., Morrison, C. D., Derbenev, A. V., Zsombok, A., & Münzberg, H. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0213-16.2016 · Cited by 159 · see citing works
Gordon, C. J., Becker, P., & Ali, J. S. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00148-6 · Cited by 146 · see citing works
Leptin regulation of hippocampal synaptic function in health and disease
Irving, A. J., & Harvey, J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0155 · Cited by 123 · see citing works
Genetic identity of thermosensory relay neurons in the lateral parabrachial nucleus
Geerling, J. C., Kim, M., Mahoney, C. E., Abbott, S. B. G., Agostinelli, L. J., Garfield, A. S., Krashes, M. J., Lowell, B. B., & Scammell, T. E. (2015) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00094.2015 · Cited by 118 · see citing works
Yahiro, T., Kataoka, N., Nakamura, Y., & Nakamura, K. (2017) · Scientific Reports · doi:10.1038/s41598-017-05327-8 · Cited by 113 · see citing works
Webb, G. P., Jagot, S. A., & Jakobson, M. (1982) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(82)90035-4 · Cited by 109 · see citing works
Sleep, vigilance, and thermosensitivity
Romeijn, N., Raymann, R. J. E. M., Møst, E., Te Lindert, B., Van Der Meijden, W. P., Fronczek, R., Gomez-Herrero, G., & Van Someren, E. J. W. (2012) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-011-1042-2 · Cited by 105 · see citing works
Hyperthermia induces c-fos expression in the preoptic area
Scammell, T. E., Price, K., & Sagar, S. M. (1993) · Brain Research · doi:10.1016/0006-8993(93)91280-6 · Cited by 94 · see citing works
Reconstruction of vocal interactions in a group of small songbirds
Anisimov, V. N., Herbst, J. A., Abramchuk, A. N., Латанов, А. В., Hahnloser, R. H. R., & Vyssotski, A. L. (2014) · Nature Methods · doi:10.1038/nmeth.3114 · Cited by 82 · see citing works
Self-citationTo sleep or not to sleep: neuronal and ecological insights
Eban-Rothschild, A., Giardino, W. J., & de Lecea, L. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.04.010 · Cited by 80 · see citing works
Temperature dependence of EEG frequencies during natural hypothermia
Deboer, T., & Tobler, I. (1995) · Brain Research · doi:10.1016/0006-8993(94)01299-w · Cited by 75 · see citing works
Abbott, S. B. G., & Saper, C. B. (2017) · The Journal of Physiology · doi:10.1113/jp274667 · Cited by 74 · see citing works
Martire, V. L., Silvani, A., Bastianini, S., Berteotti, C., & Zoccoli, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047032 · Cited by 65 · see citing works
Sleep and Waking Have a Major Effect on the 24-Hr Rhythm of Cortical Temperature in the Rat
Franken, P., Tobler, I., & Borbély, A. A. (1992) · Journal of Biological Rhythms · doi:10.1177/074873049200700407 · Cited by 63 · see citing works
Selective increases in non-rapid eye movement sleep following whole body heating in rats
Morairty, S. R., Szymusiak, R. S., Thomson, D., & McGinty, D. (1993) · Brain Research · doi:10.1016/0006-8993(93)90606-n · Cited by 56 · see citing works
Automated sleep staging in rat with a standard spreadsheet
Costa‐Miserachs, D., Portell-Cortés, I., Torras-García, M., & Morgado-Bernal, I. (2003) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(03)00229-2 · Cited by 54 · see citing works
Cellular populations and thermosensing mechanisms of the hypothalamic thermoregulatory center
Siemens, J., & Kamm, G. B. (2018) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-017-2101-0 · Cited by 50 · see citing works
Szentirmai, É., & Kapás, L. (2017) · Scientific Reports · doi:10.1038/s41598-017-01047-1 · Cited by 44 · see citing works
Leptin-mediated ion channel regulation: PI3K pathways, physiological role, and therapeutic potential
Gavello, D., Carbone, E., & Carabelli, V. (2016) · Channels · doi:10.1080/19336950.2016.1164373 · Cited by 43 · see citing works
Szentirmai, É., & Kapás, L. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12463 · Cited by 36 · see citing works
Staying awake – a genetic region that hinders α 2 adrenergic receptor agonist‐induced sleep
Gelegen, Ç., Gent, T. C., Ferretti, V., Zhang, Z., Yustos, R., Lan, F., Yang, Q., Overington, D. W. U., Vyssotski, A. L., van Lith, H. A., et al. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12570 · Cited by 31 · see citing works
Self-citationGABA-A receptors in mPOAH simultaneously regulate sleep and body temperature in freely moving rats
Jha, S. K., Yadav, V., & Mallick, B. N. (2001) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00587-1 · Cited by 24 · see citing works
Neuronal substrates for initiation, maintenance, and structural organization of sleep/wake states
Eban-Rothschild, A., & de Lecea, L. (2017) · F1000Research · doi:10.12688/f1000research.9677.1 · Cited by 21 · see citing works
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Yu, X., Li, W., Ma, Y., Tossell, K., Harris, J. J., Harding, E. C., Ba, W., Miracca, G., Wang, D., Li, L., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0288-9 · Cited by 317 · see citing works
Self-citationNeurons that regulate mouse torpor
Hrvatin, S., Sun, S., Wilcox, O. F., Yao, H., Lavin-Peter, A. J., Cicconet, M., Assad, E. G., Palmer, M. E., Aronson, S., Banks, A. S., et al. (2020) · Nature · doi:10.1038/s41586-020-2387-5 · Cited by 291 · see citing works
The Temperature Dependence of Sleep
Harding, E. C., Franks, N. P., & Wisden, W. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00336 · Cited by 261 · see citing works
“The heat generated by these mechanisms could activate the sensory receptors in the skin and so trigger NREM sleep (Harding et al., 2018).”
BackgroundInfluentialSelf-citationA Motor Theory of Sleep-Wake Control: Arousal-Action Circuit
Liu, D., & Dan, Y. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-080317-061813 · Cited by 190 · see citing works
Neuro-orchestration of sleep and wakefulness
Sulaman, B. A., Wang, S., Tyan, J., & Eban-Rothschild, A. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01236-w · Cited by 160 · see citing works
The Biology of General Anesthesia from Paramecium to Primate
Kelz, M. B., & Mashour, G. A. (2019) · Current Biology · doi:10.1016/j.cub.2019.09.071 · Cited by 151 · see citing works
Galanin Neurons Unite Sleep Homeostasis and α2-Adrenergic Sedation
Ma, Y., Miracca, G., Yu, X., Harding, E. C., Miao, A., Yustos, R., Vyssotski, A. L., Franks, N. P., & Wisden, W. (2019) · Current Biology · doi:10.1016/j.cub.2019.07.087 · Cited by 126 · see citing works
Self-citationA daily temperature rhythm in the human brain predicts survival after brain injury
Rzechorzek, N. M., Thrippleton, M. J., Chappell, F. M., Mair, G., Ercole, A., Cabeleira, M. T., Rhodes, J. K. J., Marshall, I., & O'Neill, J. S. (2021) · Brain · doi:10.1093/brain/awab466 · Cited by 128 · see citing works
A specific circuit in the midbrain detects stress and induces restorative sleep
Yu, X., Zhao, G., Wang, D., Wang, S., Li, R., Li, A., Wang, H., Nollet, M., Chun, Y. Y., Zhao, T., et al. (2022) · Science · doi:10.1126/science.abn0853 · Cited by 123 · see citing works
Self-citationA hypothalamomedullary network for physiological responses to environmental stresses
Nakamura, K., Nakamura, Y., & Kataoka, N. (2021) · Nature Reviews Neuroscience · doi:10.1038/s41583-021-00532-x · Cited by 100 · see citing works
Sleep and autonomic nervous system
Zoccoli, G., & Amici, R. (2020) · Current Opinion in Physiology · doi:10.1016/j.cophys.2020.01.002 · Cited by 114 · see citing works
Harding, E. C., Franks, N. P., & Wisden, W. (2019) · Current Opinion in Physiology · doi:10.1016/j.cophys.2019.11.008 · Cited by 113 · see citing works
Self-citationRole of the Preoptic Area in Sleep and Thermoregulation
Rothhaas, R., & Chung, S. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.664781 · Cited by 98 · see citing works
Vanini, G., Bassana, M., Mast, M., Mondino, A., Cerda, I. H., Phyle, M., Chen, V., Colmenero, A. V., Hambrecht‐Wiedbusch, V. S., & Mashour, G. A. (2020) · Current Biology · doi:10.1016/j.cub.2019.12.063 · Cited by 96 · see citing works
Control of Non-REM Sleep by Midbrain Neurotensinergic Neurons
Zhong, P., Zhang, Z., Barger, Z., Ma, C., Liu, D., Ding, X., & Dan, Y. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.026 · Cited by 93 · see citing works
Interactions between central nervous system and peripheral metabolic organs
Zeng, W., Yang, F., Shen, W. L., Zhan, C., Zheng, P., & Hu, J. (2022) · Science China Life Sciences · doi:10.1007/s11427-021-2103-5 · Cited by 96 · see citing works
Sleep in Drosophila and Its Context
Beckwith, E. J., & French, A. S. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01167 · Cited by 90 · see citing works
EP3R-Expressing Glutamatergic Preoptic Neurons Mediate Inflammatory Fever
Machado, N., Bandaru, S. S., Abbott, S. B. G., & Saper, C. B. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2887-19.2020 · Cited by 86 · see citing works
Parabrachial neuron types categorically encode thermoregulation variables during heat defense
Yang, W. Z., Du, X., Zhang, W., Gao, C., Xie, H., Xiao, Y., Jia, X., Liu, J., Xu, J., Fu, X., et al. (2020) · Science Advances · doi:10.1126/sciadv.abb9414 · Cited by 80 · see citing works
An Excitatory Circuit in the Perioculomotor Midbrain for Non-REM Sleep Control
Zhang, Z., Zhong, P., Hu, F., Barger, Z., Ren, Y., Ding, X., Li, S., Weber, F., Chung, S., Palmiter, R. D., et al. (2019) · Cell · doi:10.1016/j.cell.2019.03.041 · Cited by 79 · see citing works
Tossell, K., Yu, X., Giannos, P., Soto, B. A., Nollet, M., Yustos, R., Miracca, G., Vicente, M., Miao, A., Hsieh, B., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01430-4 · Cited by 82 · see citing works
Self-citationPreoptic BRS3 neurons increase body temperature and heart rate via multiple pathways
Piñol, R. A., Mogul, A. S., Hadley, C. K., Saha, A., Li, C., Škop, V., Province, H. S., Xiao, C., Gavrilova, O., Krashes, M. J., et al. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.05.001 · Cited by 76 · see citing works
Cardiovascular baroreflex circuit moonlights in sleep control
Yao, Y., Barger, Z., Doost, M. S., Tso, C. F., Darmohray, D. M., Silverman, D., Liu, D., Ma, C., Cetin, A. H., Yao, S., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.08.027 · Cited by 75 · see citing works
The inescapable drive to sleep: Overlapping mechanisms of sleep and sedation
Franks, N. P., & Wisden, W. (2021) · Science · doi:10.1126/science.abi8372 · Cited by 73 · see citing works
Self-citationKomagata, N., Latifi, B., Rusterholz, T., Bassetti, C. L., Adamantidis, A., & Schmidt, M. H. (2019) · Current Biology · doi:10.1016/j.cub.2019.05.009 · Cited by 63 · see citing works
Norris, A. J., Shaker, J. R., Cone, A. L., Ndiokho, I., & Bruchas, M. R. (2021) · eLife · doi:10.7554/elife.60779 · Cited by 61 · see citing works
Nakamura, Y., Yahiro, T., Fukushima, A., Kataoka, N., Hioki, H., & Nakamura, K. (2022) · Science Advances · doi:10.1126/sciadv.add5463 · Cited by 61 · see citing works
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Tsuneoka, Y., & Funato, H. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.649159 · Cited by 57 · see citing works
Zhou, Q., Fu, X., Xu, J., Dong, S., Liu, C., Cheng, D., Gao, C., Huang, M., Liu, Z., Ni, X., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.11.008 · Cited by 56 · see citing works
Mondino, A., Hambrecht‐Wiedbusch, V. S., Li, D., York, A. K., Pal, D., González, J., Torterolo, P., Mashour, G. A., & Vanini, G. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2718-20.2021 · Cited by 52 · see citing works
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Yang, W. Z., Xie, H., Du, X., Zhou, Q., Xiao, Y., Zhao, Z., Jia, X., Xu, J., Zhang, W., Cai, S., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40504-6 · Cited by 54 · see citing works
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Reitz, S. L., Wasilczuk, A. Z., Beh, G. H., Proekt, A., & Kelz, M. B. (2020) · Current Biology · doi:10.1016/j.cub.2020.10.050 · Cited by 46 · see citing works
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Machado, N., & Saper, C. B. (2021) · Temperature · doi:10.1080/23328940.2021.1993734 · Cited by 42 · see citing works
Tam, S. K. E., Brown, L. A., Wilson, T. S., Tir, S., Fisk, A. S., Pothecary, C. A., van der Vinne, V., Foster, F., Vyazovskiy, V. V., Bannerman, D. M., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2101591118 · Cited by 40 · see citing works
SEMYACHKINA-GLUSHKOVSKAYA, O. V., Fedosov, I. V., Penzel, T., Li, D., Yu, T., Telnova, V., Исмаиловна, К. Э., Saranceva, E. I., Terskov, A. V., Khorovodov, A. P., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043221 · Cited by 41 · see citing works
Be cool to be far: Exploiting hibernation for space exploration
Cerri, M., Hitrec, T., Luppi, M., & Amici, R. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.037 · Cited by 38 · see citing works
QPLOT Neurons—Converging on a Thermoregulatory Preoptic Neuronal Population
Upton, B. A., D’Souza, S. P., & Lang, R. A. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.665762 · Cited by 38 · see citing works
Effects of clozapine-N-oxide and compound 21 on sleep in laboratory mice
Traut, J., Prius-Mengual, J., Meijer, E. J., McKillop, L. E., Alfonsa, H., Hoerder‐Suabedissen, A., Song, S. H., Fehér, K. D., Riemann, D. W., Molnár, Z., et al. (2023) · eLife · doi:10.7554/elife.84740 · Cited by 37 · see citing works
Latifi, B., Adamantidis, A., Bassetti, C. L., & Schmidt, M. H. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00790 · Cited by 36 · see citing works
A temperature-regulated circuit for feeding behavior
Qian, S., Yan, S., Pang, R., Zhang, J., Liu, K., Shi, Z., Wang, Z., Chen, P., Zhang, Y., Luo, T., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31917-w · Cited by 34 · see citing works
Mitochondrial control of sleep
Hartmann, C., & Kempf, A. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102733 · Cited by 34 · see citing works
Vitazkova, D., Kosnacova, H., Turonova, D., Foltan, E., Jagelka, M., Berki, M., Micjan, M., Kokavec, O., Gerhat, F., & Vavrinský, E. (2025) · Biosensors · doi:10.3390/bios15020117 · Cited by 34 · see citing works
Yonghak, P., Miyata, S., & Kurganov, E. (2020) · Scientific Reports · doi:10.1038/s41598-020-65703-9 · Cited by 32 · see citing works
Vanini, G., & Torterolo, P. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-61663-2_5 · Cited by 30 · see citing works
Yu, X., Ma, Y., Harding, E. C., Yustos, R., Vyssotski, A. L., Franks, N. P., & Wisden, W. (2019) · SLEEP · doi:10.1093/sleep/zsz031 · Cited by 28 · see citing works
Self-citationCentral Mechanisms of Thermoregulation and Fever in Mammals
Nakamura, K. (2024) · Advances in experimental medicine and biology · doi:10.1007/978-981-97-4584-5_10 · Cited by 25 · see citing works
Zhang, Y., Li, H., Zhang, X., Wang, S., Wang, D., Wang, J., Tong, T., Zhang, Z., Yang, Q., & Dong, H. (2022) · Neuroscience Bulletin · doi:10.1007/s12264-022-00825-w · Cited by 25 · see citing works
Sleep and the recovery from stress
Yu, X., Nollet, M., Franks, N. P., & Wisden, W. (2025) · Neuron · doi:10.1016/j.neuron.2025.04.028 · Cited by 27 · see citing works
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Ambler, M. T., Hitrec, T., & Pickering, A. E. (2021) · Wellcome Open Research · doi:10.12688/wellcomeopenres.17379.1 · Cited by 22 · see citing works
TMEM16C is involved in thermoregulation and protects rodent pups from febrile seizures
Wang, T. A., Chen, C., Huang, F., Feng, S., Tien, J., Bráz, J. M., Basbaum, A. I., Jan, Y. N., & Jan, L. Y. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2023342118 · Cited by 22 · see citing works
How Temperature Influences Sleep
Fan, Y., Wang, Y., Gu, P., Han, J., & Tian, Y. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012191 · Cited by 22 · see citing works
Whole‐brain monosynaptic inputs to lateral periaqueductal gray glutamatergic neurons in mice
Ma, W., Li, L., Kong, L., Zhang, H., Yuan, P., Huang, Z., & Wang, Y. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14338 · Cited by 20 · see citing works
Hydrogen peroxide in midbrain sleep neurons regulates sleep homeostasis
Tian, Y., Kang, L., Ha, N. T., Deng, J., & Liu, D. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.04.016 · Cited by 19 · see citing works
Tai, Y., Obayashi, K., Yamagami, Y., & Saeki, K. (2023) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.10590 · Cited by 18 · see citing works
Preoptic Area Modulation of Arousal in Natural and Drug Induced Unconscious States
Reitz, S. L., & Kelz, M. B. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.644330 · Cited by 18 · see citing works
Frare, C., Jenkins, M. E., McClure, K., & Drew, K. L. (2019) · Journal of Neurochemistry · doi:10.1111/jnc.14814 · Cited by 19 · see citing works
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Nollet, M., Franks, N. P., & Wisden, W. (2023) · Journal of Huntington s Disease · doi:10.3233/jhd-230564 · Cited by 17 · see citing works
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Rogers, J. F., Vandendoren, M., Prather, J. F., Landen, J. G., Bedford, N. L., & Nelson, A. C. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105667 · Cited by 20 · see citing works
McKinley, M. J., Pennington, G. L., & Ryan, P. J. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819975-6.00028-5 · Cited by 15 · see citing works
Tossell, K., Yu, X., Soto, B. A., Vicente, M., Miracca, G., Giannos, P., Miao, A., Hsieh, B., Ma, Y., Yustos, R., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.01.179671 · Cited by 15 · see citing works
Self-citationHyperhidrosis in sleep disorders – A narrative review of mechanisms and clinical significance
Idiáquez, J., Casar, J. C., Arnardóttir, E. S., August, E., Santín, J., & Iturriaga, R. (2022) · Journal of Sleep Research · doi:10.1111/jsr.13660 · Cited by 16 · see citing works
Rivas, M., Serantes, D., Peña, F., González, J., Ferreira, A., Torterolo, P., & Benedetto, L. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.08.034 · Cited by 13 · see citing works
Rapid Eye Movement Sleep Engages Melanin-Concentrating Hormone Neurons to Reduce Cocaine Seeking
Guo, R., Wang, Y., Yan, R., Chen, B., Ding, W., Gorczyca, M. T., Ozsoy, S., Cai, L., Hines, R. L., Tseng, G. C., et al. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.06.006 · Cited by 13 · see citing works
Thermoregulation and Sleep: Functional Interaction and Central Nervous Control
Cerri, M., & Amici, R. (2021) · Comprehensive physiology · doi:10.1002/cphy.c140012 · Cited by 21 · see citing works
The how and why of sleep: Motor theory and catecholamine hypothesis
Ma, C., & Dan, Y. (2025) · Neuron · doi:10.1016/j.neuron.2025.08.017 · Cited by 13 · see citing works
Disrupting flight increases sleep and identifies a novel sleep-promoting pathway in Drosophila
Melnattur, K. V., Zhang, B., & Shaw, P. J. (2020) · Science Advances · doi:10.1126/sciadv.aaz2166 · Cited by 12 · see citing works
Harding, E. C., Ba, W., Zahir, R., Yu, X., Yustos, R., Hsieh, B., Lignos, L., Vyssotski, A. L., Merkle, F. T., Constandinou, T. G., et al. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.709825 · Cited by 12 · see citing works
Self-citationAmbient chemical and physical approaches for the modulation of sleep and wakefulness
Wang, Y., Ma, W., Kong, L.-X., Zhang, H., Yuan, P., Qu, W., Liu, C., & Huang, Z. (2024) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2024.102015 · Cited by 11 · see citing works
Li, J., Zhou, Z., Wu, Y., Zhao, J., Duan, H.-K., Peng, Y., Wang, X., Fan, Z., Yin, L., Li, M., et al. (2024) · Theranostics · doi:10.7150/thno.101422 · Cited by 11 · see citing works
Nest-building behavior in laboratory mice: Multifunctional roles and neural mechanisms
Tagawa, N., Tsuneoka, Y., & Funato, H. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106377 · Cited by 10 · see citing works
Kennedy, K. E. R., Wills, C. C. A., Holt, C., & Grandner, M. A. (2023) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.10648 · Cited by 10 · see citing works
The physiological signature of daily torpor is not orexin dependent
Martire, V. L., Berteotti, C., Bastianini, S., Alvente, S., Valli, A., Cerri, M., Amici, R., Silvani, A., Swoap, S. J., & Zoccoli, G. (2020) · Journal of Comparative Physiology B · doi:10.1007/s00360-020-01281-6 · Cited by 10 · see citing works
Thermoregulation and Sleep: Functional Interaction and Central Nervous Control
Cerri, M., & Amici, R. (2021) · Comprehensive physiology · doi:10.1002/j.2040-4603.2021.tb00151.x · Cited by 9 · see citing works
Wu, J., Liu, D.-Q., Li, J., Sun, J., Huang, Y., Zhang, S., Gao, S., & Mei, W. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210225152728 · Cited by 8 · see citing works
Soto, B. A., Ma, Y., Nollet, M., Wong, S., Miracca, G., Rastinejad, D., Yustos, R., Vyssotski, A. L., Franks, N. P., & Wisden, W. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2422878122 · Cited by 10 · see citing works
Self-citationAltered Experienced Thermoregulation in Depression—No Evidence for an Effect of Early Life Stress
von Salis, S., Ehlert, U., & Fischer, S. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.620656 · Cited by 8 · see citing works
Yu, X., Franks, N. P., & Wisden, W. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-81147-1_5 · Cited by 8 · see citing works
Self-citationHaniffa, S., Narain, P., Hughes, M. A., Petković, A., Šušić, M., Mlambo, V. C., & Chaudhury, D. (2023) · Open Biology · doi:10.1098/rsob.220380 · Cited by 6 · see citing works
A physical understanding and quantification for the regulation of orexin on sleep
Yao, C., Xu, F., Tang, X., Zou, W., Yang, D., & Shuai, J. (2023) · Chaos An Interdisciplinary Journal of Nonlinear Science · doi:10.1063/5.0156090 · Cited by 7 · see citing works
A parabrachial-hypothalamic parallel circuit governs cold defense in micePreprint
Yang, W. Z., Xie, H., Du, X., Zhou, Q., Xiao, Y., Zhao, Z., Jia, X., Xu, J., Zhang, W., Cai, S., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.19.537288 · Cited by 7 · see citing works
NREM Sleep Regulation From Neuronal Assembly to Ion
Gompf, H. S., & Anaclet, C. (2019) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-813743-7.00009-8 · Cited by 6 · see citing works
Wisden, W., & Franks, N. P. (2020) · Science · doi:10.1126/science.aba4485 · Cited by 6 · see citing works
Self-citationXu, C., Xie, Y., Zhong, T., Liang, S., Guan, H., Long, Z., Cao, H., Xing, L., Xue, X., & Zhan, Y. (2022) · Nanoscale · doi:10.1039/d2nr03115a · Cited by 5 · see citing works
ThermoMaze behavioral paradigm for assessing immobility-related brain events in rodentsPreprint
Vöröslakos, M., Zhang, Y., McClain, K., Huszár, R., Rothstein, A., & Buzsáki, G. (2023) · eLife · doi:10.7554/elife.90347 · Cited by 5 · see citing works
Role of the substantia nigra pars reticulata in sleep-wakefulness: A review of research progress
Liang, E., Chen, Y., Yan, Y., Wang, S., Yuan, J., & Yu, T. (2023) · Sleep Medicine · doi:10.1016/j.sleep.2023.11.035 · Cited by 4 · see citing works
The Art of Chilling Out: How Neurons Regulate Torpor
Ohba, A., & Yamaguchi, H. (2024) · BioEssays · doi:10.1002/bies.202400190 · Cited by 4 · see citing works
Regulation of REM and NREM sleep by preoptic glutamatergic neurons
Mondino, A., Jadidian, A., Toth, B. A., Hambrecht‐Wiedbusch, V. S., Floran-Garduno, L., Li, D., York, A. K., Torterolo, P., Pal, D., Burgess, C. R., et al. (2025) · SLEEP · doi:10.1093/sleep/zsaf141 · Cited by 4 · see citing works
Tai, Y., Obayashi, K., Yamagami, Y., & Saeki, K. (2025) · Sleep Health · doi:10.1016/j.sleh.2025.07.008 · Cited by 4 · see citing works
Neuroplasticity and brain health: insights from natural torpor
Shi, Z., Wang, X., Duan, W., Du, Y., Ling, S., Zhang, Z., Wang, G., Zhao, D., Ding, J., Zhang, K., et al. (2025) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.70069 · Cited by 4 · see citing works
A brain–body perspective on thermoregulatory adaptation
Aten, S., Lynch, N. A., Saper, C. B., & Machado, N. (2025) · Current Biology · doi:10.1016/j.cub.2025.09.023 · Cited by 4 · see citing works
Sleep: The Very Long Posited (VLPO) Synaptic Pathways of Arousal
Lüthi, A. (2019) · Current Biology · doi:10.1016/j.cub.2019.11.012 · Cited by 4 · see citing works
Neuroscience: A ‘Skin Warming’ Circuit that Promotes Sleep and Body Cooling
Peever, J. H. (2018) · Current Biology · doi:10.1016/j.cub.2018.06.043 · Cited by 4 · see citing works
Physiological Changes in the Autonomic Nervous System During Sleep
Amici, R., & Zoccoli, G. (2021) · Springer eBooks · doi:10.1007/978-3-030-62263-3_5 · Cited by 4 · see citing works
Physiological roles of reactive oxygen species in sleep homeostasis
Tian, Y., Liu, X., & Liu, D. (2025) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2025.10.273 · Cited by 3 · see citing works
van der Vinne, V., McKillop, L. E., Wilcox, S. L., Cantley, J., Peirson, S. N., Swoap, S. J., & Vyazovskiy, V. V. (2024) · Journal of Comparative Physiology B · doi:10.1007/s00360-024-01554-4 · Cited by 3 · see citing works
Satoh, A. (2022) · Springer eBooks · doi:10.1007/978-981-16-7977-3_18 · Cited by 2 · see citing works
Rocking during sleep reduces motor deficits and beta-amyloid levels in an Alzheimer’s mouse model
Zhang, L., Santoni, L., Ngo, N. A., Simayi, R., Ficiarà, E., de Vivo, L., & Bellesi, M. (2025) · iScience · doi:10.1016/j.isci.2025.112036 · Cited by 2 · see citing works
Roach, S. T., Ford, M., Simhambhatla, V., Loutrianakis, V., Farah, H., Li, Z., Periandri, E. M., Abdalla, D., Huang, I., Kalra, A., et al. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1175478 · Cited by 2 · see citing works
Riera, C. E. (2024) · Diabetes · doi:10.2337/db23-0706 · Cited by 1 · see citing works
- Authors
- Harding, E. C., Yu, X., Miao, A., Andrews, N., Ma, Y., Ye, Z., Lignos, L., Miracca, G., Ba, W., Yustos, R., Vyssotski, A. L., Wisden, W., & Franks, N. P.
- Affiliations
- Imperial College London (GB)
- UK Dementia Research Institute (GB)
- University of Zurich (CH)
- Corresponding author
- Wisden, William
- Franks, Nicholas P.
- ORCID
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2018-07
- Volume
- 28
- Issue
- 14
- Pages
- 2263-2273.e4
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC6078908
- OpenAlex
- W2883713442
- Cited by
- 136
- References
- 56
- Citations by year
- 2026: 18 · 2025: 15 · 2024: 10 · 2023: 16 · 2022: 19 · 2021: 28 · 2020: 12 · 2019: 15 · 2018: 3
- FWCI
- 8.62
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Spiral (Imperial College London) (submittedVersion, cc-by)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by)
- ETH Zürich Research Collection (cc-by)
- Funders
- BBSRC (BB/F017324/1, 00093987, 2016/ALW/00093987, BB/L015129/1)
- Netherlands Organisation for Scientific Research (019.161LW.010)
- UK Dementia Research Institute
- UK Medical Research Council
- Alzheimer's Society
- Alzheimer’s Research UK
- UK Dementia
- Wellcome Trust (107839/Z/15/Z, 107841/Z/15/Z, 104931/Z/14/Z)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Keywords
- sleep initiation, NREM sleep, body cooling, preoptic hypothalamus, GABAergic neurons, neural circuits, energy conservation, brain temperature
- MeSH terms
- Adaptation, Physiological, Animals, Body Temperature Regulation, Cold Temperature, Hot Temperature, Male, Mice, Inbred C57BL, Neurons, Preoptic Area, Sleep, Proto-Oncogene Proteins c-fos, Mice
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