Single unit activity of the suprachiasmatic nucleus and surrounding neurons during the wake-sleep cycle in mice

Neuroscience

Volumn 260, Issue , 2014, Pages 249-264

  Sakai, K ^a  

^a UNIVERSITÉ LYON 1   (France)

Author keywords

Functional heterogeneity; Single unit recording; Subparaventricular zone; Suprachiasmatic nucleus; Topographic organization; Wake sleep cycle

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL TYPE; CIRCADIAN RHYTHM; CONTROLLED STUDY; EXTRACELLULAR MATRIX; MALE; MOUSE; NERVE CELL; NERVE CELL MEMBRANE POTENTIAL; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; REM SLEEP; SLEEP PATTERN; SLEEP WAKING CYCLE; SUPRACHIASMATIC NUCLEUS; VISUAL NERVOUS SYSTEM; WAKEFULNESS;

3,3′-DIAMINOBENZIDINE; ACTIVE WAKING; AFTER-HYPERPOLARIZATION; AHA; AHPS; ANTERIOR HYPOTHALAMIC AREA; ARGININE VASOPRESSIN; AVP; AW; COEFFICIENT OF VARIATION OF THE SPIKE INTERVAL; CV; D; DAB; DROWSY STATE; EEG; ELECTROENCEPHALOGRAM; ELECTROMYOGRAM; EMG; FUNCTIONAL HETEROGENEITY; GABA; GAD; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; IMF; INSTANTANEOUS MEAN FREQUENCY; LA; LATEROANTERIOR HYPOTHALAMIC NUCLEUS; LIGHT AND DEEP SLOW-WAVE SLEEP, RESPECTIVELY; MEAN FREQUENCY; MEDIAL PREOPTIC NUCLEUS; MF; MPO; NB; NEUROBIOTIN; PARADOXICAL SLEEP; PB; PBST; PHOSPHATE BUFFER; PHOSPHATE-BUFFERED SALINE CONTAINING 0.3% TRITON X-100; PS; PST; QUIET WAKING; QW; S1 AND S2; SCN; SD; SEM; SINGLE UNIT RECORDING; SLOW-WAVE SLEEP; SPZ; STANDARD DEVIATION; STANDARD ERROR OF THE MEAN; SUBPARAVENTRICULAR ZONE; SUPRACHIASMATIC NUCLEUS; SWS; TOPOGRAPHIC ORGANIZATION; TRANSITION PERIOD FROM SLOW-WAVE SLEEP TO PS; VASOACTIVE INTESTINAL PEPTIDE; VIP; W; WAKE/SLEEP CYCLE; WAKEFULNESS;

ACTION POTENTIALS; ANIMALS; MALE; MICE; MICE, INBRED C57BL; NEURONS; SLEEP STAGES; SUPRACHIASMATIC NUCLEUS; WAKEFULNESS;

EID: 84892496774     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.12.020     Document Type: Article

References (69)

1. Abrahamson E.E., Moore R.Y. Suprachiasmatic nucleus in the mouse: retinal innervation, intrinsic organization and efferent projections. Brain Res 2001, 916:172-191.
2. Abrahamson E.E., Moore R.Y. Lesions of suprachiasmatic nucleus efferents selectively affect rest-activity rhythm. Mol Cell Endocrinol 2006, 252:46-56.
3. Airaksinen M.S., Alanen S., Szabat E., Visser T.J., Panula P. Multiple neurotransmitters in the tuberomammillary nucleus: comparison of rat, mouse, and guinea pig. J Comp Neurol 1992, 323:103-116.
4. Albus H., Vansteensel M.J., Michel S., Block G.D., Meijer J.H. A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol 2005, 15:886-893.
5. Asala S.A., Okano Y., Honda K., Inoue S. Effects of medial preoptic lesions on sleep and wakefulness in unrestrained rats. Neurosci Lett 1990, 114:300-304.
6. Belenky M.A., Wagner S., Yarom Y., Matzner H., Cohen S., Castel M. The suprachiasmatic nucleus in stationary organotypic culture. Neuroscience 1996, 70:127-143.
7. Buijs R.M., Wortel J., Hou Y.X. Colocalization of gamma-aminobutyric acid with vasopressin, vasoactive intestinal peptide, and somatostatin in the rat suprachiasmatic nucleus. J Comp Neurol 1995, 358:343-352.
8. Castel M., Morris J.F. Morphological heterogeneity of the GABAergic network in the suprachiasmatic nucleus, the brain's circadian pacemaker. J Anat 2000, 196:1-13.
9. Deboer T., Vansteensel M.J., Détári L., Meijer J.H. Sleep states alter activity of suprachiasmatic nucleus neurons. Nat Neurosci 2003, 6:1086-1090.
10. Earnest D.J., Sladek C.D. Circadian vasopressin release from perifused rat suprachiasmatic explants in vitro: effects of acute stimulation. Brain Res 1987, 422:398-402.
11. Edgar D.M., Dement W.C., Fuller C.A. Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J Neurosci 1993, 13:1065-1079.
12. Ericson H., Köhler C., Blomqvist A. GABA-like immunoreactivity in tuberomammillary nucleus: an electron microscopic study in the rat. J Comp Neurol 1991, 305:462-469.
13. Glotzbach S.F., Cornett C.M., Heller H.C. Activity of suprachiasmatic and hypothalamic neurons during sleep and wakefulness in the rat. Brain Res 1987, 419:279-286.
14. Green D.J., Gillette R. Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res 1982, 245:198-200.
15. Groos G.A., Hendriks J. Regularly firing neurons in the rat suprachiasmatic nucleus. Experientia 1979, 35:1597-1598.
16. Groos G.A., Hendriks J. Circadian rhythms in electrical discharge of rat suprachiasmatic neurons recorded in vitro. Neurosci Lett 1982, 34:283-288.
17. Ibuka N., Inouye S.I., Kawamura H. Analysis of sleep-wakefulness rhythms in male rats after suprachasmatic nucleus lesions and ocular enucleation. Brain Res 1977, 122:33-47.
18. Ibuka N., Kawamura H. Loss of circadian rhythm in sleep-wakefulness cycle in the rat by suprachiasmatic nucleus lesions. Brain Res 1975, 96:76-81.
19. Inouye S.T., Kawamura H. Persistance of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus. Proc Nath Acad Sci USA 1979, 76:5962-5966.
20. Jiang Z.G., Yang Y.Q., Liu Z.P., Allen C.N. Membrane properties and synaptic inputs of the suprachiasmatic nucleus in rat brain slices. J Physiol 1997, 499:141-159.
21. Kim Y.I., Dudek F.E. Membrane properties of rat suprachiasmatic nucleus neurons receiving optic nerve input. J Physiol 1993, 464:229-243.
22. Kow L.M., Pfaff D.W. Suprachiasmatic neurons in tissue slices from ovariectomized rats: electrophysiological and neuropharmacological characterization and the effects of estrogen treatment. Brain Res 1984, 297:275-286.
23. Kubota A., Inouye S.I., Kawamura H. Reversal of multiunit activity within and outside the SCN in the rat. Neurosci Lett 1981, 27:303-308.
24. Leak R.K., Moore R.Y. Topographic organization of suprachiasmatic nucleus projection neurons. J Comp Neurol 2001, 433:312-334.
25. Liu C., Reppert S.M. GABA synchronizes clock cells within the suprachiasmatic circadian clock. Neuron 2000, 25:123-128.
26. Lu J., Zhang Y.H., Chou T.C., Gaus S.E., Elmquist J.K., Shiromani P., Saper C.B. Contrasting effects of ibotenate lesions of the paraventricular nucleus and subparaventricular zone on sleep-wake cycle and temperature regulation. J Neurosci 2001, 21:4864-4874.
27. Manns I.D., Alonso A., Jones B.E. Discharging profiles of juxtacellularly labeled and immunohistochemically identified GABAergic basal forebrain neurons recorded in association with the electroencephalogram in anesthetized rats. J Neurosci 2000, 20:9252-9263.
28. Manns I.D., Alonso A., Jones B.E. Rhythmically discharging basal forebrain units comprise cholinergic, GABAergic, and putative glutamatergic cells. J Neurophysiol 2003, 89:1057-1066.
29. Mistlberger R.E. Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res Rev 2005, 49:429-454.
30. Mistlberger R.E., Bergmann B.M., Waldenar W., Rechtschaffen A. Recovery sleep following sleep deprivation in intact and suprachiasmatic nuclei lesioned rats. Sleep 1983, 6:217-233.
31. Moore R.Y., Speh J.C. GABA is the principal neurotransmitter of the circadian system. Neurosci Lett 1993, 150:112-116.
32. Moore R.Y., Speh J.C., Leak R.K. Suprachiasmatic nucleus organization. Cell Tissue Res 2002, 309:89-98.
33. Morin L.P., Shivers K.Y., Blanchard J.H., Muscat L. Complex organization of mouse and rat suprachiasmatic nucleus. Neuroscience 2006, 137:1285-1297.
34. Mouret J., Coindet J., Debilly G., Chouvet G. Suprachiasmatic nuclei lesions in the rat: alterations in sleep circadian rhythms. Electroenceph Clin Neurophysiol 1978, 45:402-408.
35. Murakami N., Takamure M., Takahashi K., Utunomiya K., Kuroda H., Etoh T. Long-term cultured neurons from rat suprachiasmatic nucleus retain the capacity for circadian oscillation of vasopressin release. Brain Res 1991, 545:347-350.
36. Nakamura W., Yamazaki S., Nakamura T.J., Shirakawa T., Block G.D., Takumi T. In vivo monitoring of circadian timing in freely moving mice. Curr Biol 2008, 18:381-385.
37. Nishino H., Koizumi K. Responses of neurons in the suprachiasmatic nuclei of the hypothalamus to putative transmitters. Brain Res 1977, 120:167-172.
38. Nishino H., Koizumi K., Brooks C.M. The role of suprachiasmatic nuclei of the hypothalamus in the production of circadian rhythm. Brain Res 1976, 112:45-59.
39. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2001, Academic Press, San Diego.
40. Pennartz C.M.A., Bos N., De Jeu M.T.G., Gueursten A.M.S., Mirmiran M., Sluiter A.A., Buijs R.M. Membrane properties and morphology of vasopressin neurons in slices of rat suprachiasmatic nucleus. J Physiol 1998, 80:2710-2717.
41. Pennartz C.M.A., De Jeu M.T.G., Geurtsen A.M.S., Sluiter A.A., Hermes M.L.H.J. Electrophysiological and morphological heterogeneity of neurons in slices of rat suprachiasmatic nucleus. J Physiol 1998, 563:775-793.
42. Pinault D. A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellular labeled thalamic cells and other central neurons with biocytin or neurobiotin. J Neurosci Meth 1996, 65:113-136.
43. Sakai K. Sleep-waking discharge profiles of median preoptic and surrounding neurons in mice. Neuroscience 2011, 182:144-161.
44. Sakai K. Sleep-waking discharge profiles of dorsal raphe nucleus neurons in mice. Neuroscience 2011, 197:200-224.
45. Sakai K. Discharge properties of presumed cholinergic and noncholinergic laterodorsal tegmental neurons related to cortical activation in non-anesthetized mice. Neuroscience 2012, 224:172-190.
46. Sakai K., Takahashi K., Anaclet C., Lin J.S. Sleep-waking discharge of ventral tuberomammillary neurons in wild-type and histidine decarboxylase knock-out mice. Front Behav Neurosci 2010, 4:1-10.
47. Saper C.B., Lu J., Chou T.C., Gooley J. The hypothalamic integrator for circadian rhythms. Trends Neurosci 2005, 28:152-157.
48. Schmidt M.H., Valatx J.L., Sakai K., Fort P., Jouvet M. Role of the lateral preoptic area in sleep-related erectile mechanisms and sleep generation in the rat. J Neurosci 2000, 20:6640-6647.
49. Shibata S., Liou S.Y., Ueki S., Oomura Y. Influence of environmental light-dark cycle and enucleation on activity of suprachiasmatic neurons in slice preparation. Brain Res 1984, 302:75-81.
50. Shibata S., Oomura Y., Kita H., Hattori K. Circadian rhythmic changes of neuronal activity in the suprachiasmatic nucleus of the rat hypothalamic slice. Brain Res 1982, 247:154-158.
51. Shinohara K., Honma S., Katsuno Y., Abe H., Honma K. Two distinct oscillators in the rat suprachiasmatic nucleus in vitro. Proc Natl Acad Sci USA 1995, 92:7396-7400.
52. Shirakawa T., Honma S., Katsuno Y., Oguchi H., Honma K. Synchronization of circadian firing rhythms in cultured rat suprachiasmatic neurons. Eur J Neurosci 2000, 12:2833-2838.
53. Simon A.P., Poindessous-Jazat F., Dutar P., Epelbaum J., Bassant M.H. Firing properties of anatomically identified neurons in the medial septum of anesthetized and unanesthetized restrained rats. J Neurosci 2006, 26:9038-9046.
54. Stephan F.K., Zucker I. Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 1972, 69:1538-1586.
55. A-mediated local synaptic pathways connect neurons in the rat suprachiasmatic nucleus. J Neurophysiol 1997, 78:2217-2220.
56. Takahashi K., Lin J.S., Sakai K. Neuronal activity of histaminergic tuberomammillary neurons during wake-sleep states in the mouse. J Neurosci 2006, 26:10292-10298.
57. Takahashi K., Lin J.S., Sakai K. Characterization and mapping of sleep-waking specific neurons in the basal forebrain and preoptic hypothalamus in mice. Neuroscience 2009, 161:269-292.
58. Takahashi K., Kayama Y., Lin J.S., Sakai K. Locus coeruleus neuronal activity during the sleep-waking cycle in mice. Neuroscience 2010, 169:1115-1126.
59. Takeda N., Inagaki S., Shiosaka S., Taguchi Y., Oertel W.H., Tohyama M., Watanabe T., Wada H. Immunohistochemical evidence for the coexistence of histidine decarboxylase-like and glutamate decarboxylase-like immunoreactivities in nerve cells of the magnocellular nucleus of the posterior hypothalamus of rats. Proc Natl Acad Sci USA 1984, 81:7647-7650.
60. Tanaka M., Matsuda T., Shigeyoshi Y., Ibata Y., Okamura H. Peptide expression in GABAergic neurons in the rat suprachiasmatic nucleus in comparison with other forebrain structures: a double labeling in situ hybridization study. J Histochem Cytochem 1997, 45:1231-1237.
61. Thomson A.M. Slow, regular, discharge in suprachiasmatic neurons is calcium dependent, in slices of rat brain. Neuroscience 1984, 13:761-767.
62. Tominaga K., Shinohara K., Otori Y., Fukuhara C., Inouye S.T. Circadian rhythms of vasopressin content in the suprachiasmatic nucleus of the rat. Neuroreport 1992, 3:809-812.
63. van den Pol A.N. The hypothalamic suprachiasmatic nucleus of the rat: intrinsic anatomy. J Comp Neurol 1980, 191:661-702.
64. Vincent S.R., Hökfelt T., Skirboll L.R., Wu J.Y. Hypothalamic gamma-aminobutyric acid neurons project to the cortex. Science 1983, 220:1309-1311.
65. Watts A.G., Swanson L.W. Efferent projections of the suprachiasmatic nucleus: II. Studies using retrograde transport of fluorescent dyes and simultaneous peptide immunohistochemistry in the rat. J Comp Neurol 1987, 258:230-252.
66. Watts A.G., Swanson L.W., Sanchez-Watts G. The efferent projections of the suprachiasmatic nucleus: I. Studies using anterograde transport of Phaseolus vulgaris leucoagglutinin (PHA-L) in the rat. J Comp Neurol 1987, 258:204-229.
67. Welsh D.K., Logothetis D.E., Meister M., Reppert S.M. Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms. Neuron 1995, 14:697-706.
68. Wheal H.V., Thomson A.M. The electrical properties of neurons of the rat SCN recorded intracellularly in vitro. Neuroscience 1984, 13:97-104.
69. Yamazaki S., Kerbeshian M.C., Hocker C.G., Block G.D., Menaker M. Rhythmic properties of the hamster suprachiasmatic nucleus in vivo. Neuroscience 1998, 18:10709-10723.