Identification of preoptic sleep neurons using retrograde labelling and gene profiling

Nature

Volumn 545, Issue 7655, 2017, Pages 477-481

  Chung, Shinjae ^a   Weber, Franz ^a   Zhong, Peng ^a   Tan, Chan Lek ^b   Nguyen, Thuc Nghi ^c   Beier, Kevin T ^d   Hörmann, Nikolai ^a   Chang, Wei Cheng ^a   Zhang, Zhe ^a   Do, Johnny Phong ^a   Yao, Shenqin ^c   Krashes, Michael J ^e,f   Tasic, Bosiljka ^c   Cetin, Ali ^c   Zeng, Hongkui ^c   Knight, Zachary A ^b   Luo, Liqun ^d   Dan, Yang ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^d STANFORD UNIVERSITY   (United States)

^e NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^f NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CHOLECYSTOKININ; CORTICOTROPIN RELEASING FACTOR; DYNORPHIN A; GALANIN; HISTAMINE; PROTEIN C FOS; RNA; SUBSTANCE P; TACHYKININ; VESICULAR GLUTAMATE TRANSPORTER; BIOLOGICAL MARKER; CHANNELRHODOPSIN 2, MOUSE; CHLORIDE CHANNEL; RHODOPSIN; TRANSCRIPTOME;

ACTIVATION ENERGY; CELLS AND CELL COMPONENTS; GENE; GENETIC ANALYSIS; GENETIC MARKER; HISTOLOGY; IDENTIFICATION METHOD; IMMUNOASSAY; MAMMAL; PEPTIDE; SLEEP;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FEMALE; FIRING RATE; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC MANIPULATION; HISTAMINE RELEASE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MOUSE; NERVE CELL; NONHUMAN; OPTOGENETICS; PREOPTIC AREA; PRIORITY JOURNAL; REM SLEEP; RNA PURIFICATION; RNA SEQUENCE; TUBEROMAMMILLARY NUCLEUS; WAKEFULNESS; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENETICS; LATERAL HYPOTHALAMUS; METABOLISM; NEUROANATOMICAL TRACT TRACING; PHYSIOLOGY; RADIATION RESPONSE; RIBOSOME; SEQUENCE ANALYSIS; SINGLE CELL ANALYSIS; SLEEP;

LENTIVIRUS; MAMMALIA;

ANIMALS; BIOMARKERS; CHLORIDE CHANNELS; CHOLECYSTOKININ; CORTICOTROPIN-RELEASING HORMONE; FEMALE; GABAERGIC NEURONS; HYPOTHALAMIC AREA, LATERAL; MALE; MICE; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONS; OPTOGENETICS; PREOPTIC AREA; PROTO-ONCOGENE PROTEINS C-FOS; RHODOPSIN; RIBOSOMES; SEQUENCE ANALYSIS, RNA; SINGLE-CELL ANALYSIS; SLEEP; TACHYKININS; TRANSCRIPTOME; WAKEFULNESS;

EID: 85019768638     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature22350     Document Type: Article

References (45)

1. Von Economo, C. Sleep as a problem of localization. J. Nerv. Ment. Dis. 71, 249-259 (1930).
2. Nauta, W. J. Hypothalamic regulation of sleep in rats; an experimental study. J. Neurophysiol. 9, 285-316 (1946).
3. McGinty, D. J. & Sterman, M. B. Sleep suppression after basal forebrain lesions in the cat. Science 160, 1253-1255 (1968).
4. Sallanon, M. et al. Long-lasting insomnia induced by preoptic neuron lesions and its transient reversal by muscimol injection into the posterior hypothalamus in the cat. Neuroscience 32, 669-683 (1989).
5. Lu, J., Greco, M. A., Shiromani, P. & Saper, C. B. Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J. Neurosci. 20, 3830-3842 (2000).
6. Szymusiak, R., Alam, N., Steininger, T. L. & McGinty, D. Sleep-waking discharge patterns of ventrolateral preoptic/anterior hypothalamic neurons in rats. Brain Res. 803, 178-188 (1998).
7. Takahashi, K., Lin, J. S. & Sakai, K. Characterization and mapping of sleepwaking specific neurons in the basal forebrain and preoptic hypothalamus in mice. Neuroscience 161, 269-292 (2009).
8. Gong, H. et al. Activation of c-fos in GABAergic neurones in the preoptic area during sleep and in response to sleep deprivation. J. Physiol. (Lond.) 556, 935-946 (2004).
9. Sherin, J. E., Shiromani, P. J., McCarley, R. W. & Saper, C. B. Activation of ventrolateral preoptic neurons during sleep. Science 271, 216-219 (1996).
10. Zhang, Z. et al. Neuronal ensembles sufficient for recovery sleep and the sedative actions of 2 adrenergic agonists. Nat. Neurosci. 18, 553-561 (2015).
11. Sherin, J. E., Elmquist, J. K., Torrealba, F. & Saper, C. B. Innervation of histaminergic tuberomammillary neurons by GABAergic and galaninergic neurons in the ventrolateral preoptic nucleus of the rat. J. Neurosci. 18, 4705-4721 (1998).
12. Steininger, T. L., Gong, H., McGinty, D. & Szymusiak, R. Subregional organization of preoptic area/anterior hypothalamic projections to arousal-related monoaminergic cell groups. J. Comp. Neurol. 429, 638-653 (2001).
13. Cetin, A. & Callaway, E. M. Optical control of retrogradely infected neurons using drug-regulated "TLoop" lentiviral vectors. J. Neurophysiol. 111, 2150-2159 (2014).
14. Berndt, A. et al. Structural foundations of optogenetics: determinants of channelrhodopsin ion selectivity. Proc. Natl Acad. Sci. USA 113, 822-829 (2016).
15. Beier, K. T. et al. Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping. Cell 162, 622-634 (2015).
16. Heiman, M. et al. A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748 (2008).
17. Mansbach, R. S. & Lorenz, D. N. Cholecystokinin (CCK-8) elicits prandial sleep in rats. Physiol. Behav. 30, 179-183 (1983).
18. Kimura, M. et al. Conditional corticotropin-releasing hormone overexpression in the mouse forebrain enhances rapid eye movement sleep. Mol. Psychiatry 15, 154-165 (2010).
19. Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995-1013 (2011).
20. Sternson, S. M. & Roth, B. L. Chemogenetic tools to interrogate brain functions. Annu. Rev. Neurosci. 37, 387-407 (2014).
21. Gaus, S. E., Strecker, R. E., Tate, B. A., Parker, R. A. & Saper, C. B. Ventrolateral preoptic nucleus contains sleep-active, galaninergic neurons in multiple mammalian species. Neuroscience 115, 285-294 (2002).
22. Zhang, G., Wang, L., Liu, H. & Zhang, J. Substance P promotes sleep in the ventrolateral preoptic area of rats. Brain Res. 1028, 225-232 (2004).
23. Greco, M. A. et al. Opioidergic projections to sleep-active neurons in the ventrolateral preoptic nucleus. Brain Res. 1245, 96-107 (2008).
24. Okaty, B. W., Sugino, K. & Nelson, S. B. A quantitative comparison of cell-type-specific microarray gene expression profiling methods in the mouse brain. PLoS ONE 6, e16493 (2011).
25. Weber, F. et al. Control of REM sleep by ventral medulla GABAergic neurons. Nature 526, 435-438 (2015).
26. Xu, M. et al. Basal forebrain circuit for sleep-wake control. Nat. Neurosci. 18, 1641-1647 (2015).
27. Jego, S. et al. Optogenetic identification of a rapid eye movement sleep modulatory circuit in the hypothalamus. Nat. Neurosci. 16, 1637-1643 (2013).
28. Van Dort, C. J. et al. Optogenetic activation of cholinergic neurons in the PPT or LDT induces REM sleep. Proc. Natl Acad. Sci. USA 112, 584-589 (2015).
29. Hayashi, Y. et al. Cells of a common developmental origin regulate REM/ non-REM sleep and wakefulness in mice. Science 350, 957-961 (2015).
30. Anaclet, C. et al. The GABAergic parafacial zone is a medullary slow wave sleep-promoting center. Nat. Neurosci. 17, 1217-1224 (2014).
31. Franklin, K. B. J. & Paxinos, G. in The Mouse Brain in Stereotaxic Coordinates 3rd edn, 31-52 (Academic, 2007).
32. Vong, L. et al. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71, 142-154 (2011).
33. Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140 (2010).
34. Krashes, M. J. et al. An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger. Nature 507, 238-242 (2014).
35. Terao, A., Greco, M. A., Davis, R. W., Heller, H. C. & Kilduff, T. S. Region-specific changes in immediate early gene expression in response to sleep deprivation and recovery sleep in the mouse brain. Neuroscience 120, 1115-1124 (2003).
36. Borbély, A. A., Tobler, I. & Hanagasioglu, M. Effect of sleep deprivation on sleep and EEG power spectra in the rat. Behav. Brain Res. 14, 171-182 (1984).
37. Anikeeva, P. et al. Optetrode: A multichannel readout for optogenetic control in freely moving mice. Nat. Neurosci. 15, 163-170 (2011).
38. Schmitzer-Torbert, N., Jackson, J., Henze, D., Harris, K. & Redish, A. D. Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131, 1-11 (2005).
39. Knight, Z. A. et al. Molecular profiling of activated neurons by phosphorylated ribosome capture. Cell 151, 1126-1137 (2012).
40. Mi, H., Muruganujan, A., Casagrande, J. T. & Thomas, P. D. Large-scale gene function analysis with the PANTHER classification system. Nat. Protocols 8, 1551-1566 (2013).
41. Sugino, K. et al. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat. Neurosci. 9, 99-107 (2006).
42. Hempel, C. M., Sugino, K. & Nelson, S. B. A manual method for the purification of fluorescently labeled neurons from the mammalian brain. Nat. Protocols 2, 2924-2929 (2007).
43. Tasic, B. et al. Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat. Neurosci. 19, 335-346 (2016).
44. Zhang, S. et al. Long-range and local circuits for top-down modulation of visual cortex processing. Science 345, 660-665 (2014).
45. Lambolez, B., Audinat, E., Bochet, P., Crépel, F. & Rossier, J. AMPA receptor subunits expressed by single Purkinje cells. Neuron 9, 247-258 (1992).