Neurophysiological analysis of the suprachiasmatic nucleus: A challenge at multiple levels

Methods in Enzymology

Volumn 552, Issue , 2015, Pages 75-102

  Meijer, Johanna H ^a   Michel, Stephan ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CYCLIC AMP; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NEUROPEPTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; BEHAVIOR; CELL ACTIVITY; CELL LEVEL; CELL SYNCHRONIZATION; CIRCADIAN RHYTHM; CYTOSOL; ELECTRIC ACTIVITY; ELECTROPHYSIOLOGY; FEEDBACK SYSTEM; GABAERGIC TRANSMISSION; GENE EXPRESSION; IN VIVO STUDY; LONG TERM EXPOSURE; MOLECULAR BIOLOGY; MOLECULAR CLOCK; NEGATIVE FEEDBACK; NERVE CELL; NERVE CELL NETWORK; NEUROMODULATION; NEUROPHYSIOLOGY; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; OSCILLATION; PHOTOPERIODICITY; PRIORITY JOURNAL; PROTEIN FUNCTION; SINGLE CELL ANALYSIS; SLEEP STAGE; SUPRACHIASMATIC NUCLEUS; ANESTHESIA; ANIMAL; BIOLOGICAL RHYTHM; PHYSIOLOGY;

ANESTHESIA; ANIMALS; BIOLOGICAL CLOCKS; SUPRACHIASMATIC NUCLEUS;

EID: 84923313706     PISSN: 00766879     EISSN: 15577988     Source Type: Book Series    
DOI: 10.1016/bs.mie.2014.11.001     Document Type: Chapter

References (135)

1. T. Akasu, S. Shoji, and H. Hasuo Inward rectifier and low-threshold calcium currents contribute to the spontaneous firing mechanism in neurons of the rat suprachiasmatic nucleus Pflügers Archiv 425 1-2 1993 109 116
2. U. Albrecht Timing to perfection: The biology of central and peripheral circadian clocks Neuron 74 2 2012 246 260
3. H. Albus, X. Bonnefont, I. Chaves, A. Yasui, J. Doczy, and G.T. van der Horst Cryptochrome-deficient mice lack circadian electrical activity in the suprachiasmatic nuclei Current Biology 12 13 2002 1130 1133
4. H. Albus, M.J. Vansteensel, S. Michel, G.D. Block, and J.H. Meijer A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock Current Biology 15 10 2005 886 893
5. C.M. Altimus, A.D. Gueler, N.M. Alam, A.C. Arman, G.T. Prusky, and A.P. Sampath Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities Nature Neuroscience 13 9 2010 U1102 U1107
6. L. Alvado, and C.N. Allen Tetraethylammonium (TEA) increases the inactivation time constant of the transient K + current in suprachiasmatic nucleus neurons Brain Research 1221 2008 24 29
7. M.C. Antle, and R. Silver Orchestrating time: Arrangements of the brain circadian clock Trends in Neurosciences 28 3 2005 145 151
8. K. Baba, D. Ono, S. Honma, and K. Honma A TTX-sensitive local circuit is involved in the expression of PK2 and BDNF circadian rhythms in the mouse suprachiasmatic nucleus The European Journal of Neuroscience 27 4 2008 909 916
9. M.A. Belenky, P.J. Sollars, D.B. Mount, S.L. Alper, Y. Yarom, and G.E. Pickard Cell-type specific distribution of chloride transporters in the rat suprachiasmatic nucleus Neuroscience 165 4 2010 1519 1537
10. M.A. Belenky, Y. Yarom, and G.E. Pickard Heterogeneous expression of gamma-aminobutyric acid and gamma-aminobutyric acid-associated receptors and transporters in the rat suprachiasmatic nucleus The Journal of Comparative Neurology 506 4 2008 708 732
11. G.D. Block, S.B. Khalsa, D.G. McMahon, S. Michel, and M. Geusz Biological clocks in the retina: Cellular mechanisms of biological timekeeping International Review of Cytology 146 1993 83 144
12. Y. Bouskila, and F.E. Dudek A rapidly activating type of outward rectifier K + current and A - current in rat suprachiasmatic nucleus neurones The Journal of Physiology 488 Pt 2 1995 339 350
13. 2 + axis controls circuit-level encoding of circadian time in the suprachiasmatic nucleus Neuron 78 4 2013 714 728
14. T.M. Brown, J.R. Banks, and H.D. Piggins A novel suction electrode recording technique for monitoring circadian rhythms in single and multiunit discharge from brain slices Journal of Neuroscience Methods 156 1-2 2006 173 181
15. T.M. Brown, and H.D. Piggins Spatiotemporal heterogeneity in the electrical activity of suprachiasmatic nuclei neurons and their response to photoperiod Journal of Biological Rhythms 24 1 2009 44 54
16. T.M. Brown, J. Wynne, H.D. Piggins, and R.J. Lucas Multiple hypothalamic cell populations encoding distinct visual information The Journal of Physiology 589 Pt 5 2011 1173 1194
17. E.D. Buhr, S.H. Yoo, and J.S. Takahashi Temperature as a universal resetting cue for mammalian circadian oscillators Science 330 6002 2010 379 385
18. G. Cao, J. Platisa, V.A. Pieribone, D. Raccuglia, M. Kunst, and M.N. Nitabach Genetically targeted optical electrophysiology in intact neural circuits Cell 154 4 2013 904 913
19. M. Castel, and J.F. Morris Morphological heterogeneity of the GABAergic network in the suprachiasmatic nucleus, the brain's circadian pacemaker Journal of Anatomy 196 Pt 1 2000 1 13
20. M.Y. Cheng, C.M. Bullock, C. Li, A.G. Lee, J.C. Bermak, and J. Belluzzi Prokineticin 2 transmits the behavioural circadian rhythm of the suprachiasmatic nucleus Nature 417 6887 2002 405 410
21. H.J. Choi, C.J. Lee, A. Schroeder, Y.S. Kim, S.H. Jung, and J.S. Kim Excitatory actions of GABA in the suprachiasmatic nucleus The Journal of Neuroscience 28 21 2008 5450 5459
22. C.S. Colwell Circadian modulation of calcium levels in cells in the suprachiasmatic nucleus The European Journal of Neuroscience 12 2 2000 571 576
23. C.S. Colwell Linking neural activity and molecular oscillations in the SCN Nature Reviews. Neuroscience 12 10 2011 553 569
24. C.S. Colwell, S. Michel, J. Itri, W. Rodriguez, J. Tam, and V. Lelievre Disrupted circadian rhythms in VIP- and PHI-deficient mice American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 285 5 2003 R939 R949
25. C.P. Coomans, S.A.A. van den Berg, T. Houben, J.B. van Klinken, R. van den Berg, and A.C.M. Pronk Detrimental effects of constant light exposure and high-fat diet on circadian energy metabolism and insulin sensitivity FASEB Journal 27 4 2013 1721 1732
26. L.N. Cui, and R.E.J. Dyball Synaptic input from the retina to the suprachiasmatic nucleus changes with the light-dark cycle in the Syrian hamster Journal of Physiology London 497 2 1996 483 493
27. T. Deboer, L. Detari, and J.H. Meijer Long term effects of sleep deprivation on the mammalian circadian pacemaker Sleep 30 3 2007 257 262
28. T. Deboer, M.J. Vansteensel, L. Detari, and J.H. Meijer Sleep states alter activity of suprachiasmatic nucleus neurons Nature Neuroscience 6 10 2003 1086 1090
29. M.J. Deery, E.S. Maywood, J.E. Chesham, M. Sladek, N.A. Karp, and E.W. Green Proteomic analysis reveals the role of synaptic vesicle cycling in sustaining the suprachiasmatic circadian clock Current Biology 19 23 2009 2031 2036
30. A. Depetris-Chauvin, J. Berni, E.J. Aranovich, N.I. Muraro, E.J. Beckwith, and M.F. Ceriani Adult-specific electrical silencing of pacemaker neurons uncouples molecular clock from circadian outputs Current Biology 21 21 2011 1783 1793
31. M. Diaz-Munoz, M.A. Dent, D. Granados-Fuentes, A.C. Hall, A. Hernandez-Cruz, and M.E. Harrington Circadian modulation of the ryanodine receptor type 2 in the SCN of rodents Neuroreport 10 3 1999 481 486
32. M.J. Duncan, J.M. Herron, and S.A. Hill Aging selectively suppresses vasoactive intestinal peptide messenger RNA expression in the suprachiasmatic nucleus of the Syrian hamster Brain Research Molecular Brain Research 87 2 2001 196 203
33. G.B. Ellis, R.E. McKlveen, and F.W. Turek Dark pulses affect the circadian-rhythm of activity in hamsters kept in constant light American Journal of Physiology 242 1 1982 R44 R50
34. S. Farajnia, T. Deboer, J.H. Rohling, J.H. Meijer, and S. Michel Aging of the suprachiasmatic clock The Neuroscientist 20 1 2014 44 55
35. S. Farajnia, S. Michel, T. Deboer, H.T. vanderLeest, T. Houben, and J.H. Rohling Evidence for neuronal desynchrony in the aged suprachiasmatic nucleus clock The Journal of Neuroscience 32 17 2012 5891 5899
36. L. Frenkel, and M.F. Ceriani Circadian plasticity: From structure to behavior International Review of Neurobiology 99 2011 107 138
37. M.U. Gillette The suprachiasmatic nuclei: Circadian phase-shifts induced at the time of hypothalamic slice preparation are preserved in vitro Brain Research 379 1 1986 176 181
38. M.U. Gillette, M. Medanic, A.J. McArthur, C. Liu, J.M. Ding, and L.E. Faiman Intrinsic neuronal rhythms in the suprachiasmatic nuclei and their adjustment Ciba Foundation Symposium 183 1995 134 144 discussion 144-153
39. D.J. Green, and R. Gillette Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice Brain Research 245 1 1982 198 200
40. G. Groos, and J. Hendriks Circadian rhythms in electrical discharge of rat suprachiasmatic neurones recorded in vitro Neuroscience Letters 34 3 1982 283 288
41. G.A. Groos, and R. Mason An electro-physiological study of the rats suprachiasmatic nucleus - A Locus for the action of anti-depressants Journal of Physiology London 330 1982 P40
42. S. Han, F.H. Yu, M.D. Schwartz, J.D. Linton, M.M. Bosma, and J.B. Hurley Na(V)1.1 channels are critical for intercellular communication in the suprachiasmatic nucleus and for normal circadian rhythms Proceedings of the National Academy of Sciences of the United States of America 109 6 2012 E368 E377
43. 2 + regulates free-running circadian clock oscillation in vivo The Journal of Neuroscience 27 46 2007 12489 12499
44. E.D. Herzog, S.J. Aton, R. Numano, Y. Sakaki, and H. Tei Temporal precision in the mammalian circadian system: A reliable clock from less reliable neurons Journal of Biological Rhythms 19 1 2004 35 46
45. E.D. Herzog, M.E. Geusz, S.B. Khalsa, M. Straume, and G.D. Block Circadian rhythms in mouse suprachiasmatic nucleus explants on multimicroelectrode plates Brain Research 757 2 1997 285 290
46. E.D. Herzog, and R.M. Huckfeldt Circadian entrainment to temperature, but not light, in the isolated suprachiasmatic nucleus Journal of Neurophysiology 90 2 2003 763 770
47. S. Honma, W. Nakamura, T. Shirakawa, and K. Honma Diversity in the circadian periods of single neurons of the rat suprachiasmatic nucleus depends on nuclear structure and intrinsic period Neuroscience Letters 358 3 2004 173 176
48. S. Honma, D. Ono, Y. Suzuki, N. Inagaki, T. Yoshikawa, and W. Nakamura Suprachiasmatic nucleus: Cellular clocks and networks Progress in Brain Research 199 2012 129 141
49. T. Houben, C.P. Coomans, and J.H. Meijer Regulation of circadian and acute activity levels by the murine suprachiasmatic nuclei PLoS One 9 10 2014 e110172
50. T. Houben, T. Deboer, F. van Oosterhout, and J.H. Meijer Correlation with behavioral activity and rest implies circadian regulation by SCN neuronal activity levels Journal of Biological Rhythms 24 6 2009 477 487
51. K. Hu, J.H. Meijer, S.A. Shea, H.T. vanderLeest, B. Pittman-Polletta, and T. Houben Fractal patterns of neural activity exist within the suprachiasmatic nucleus and require extrinsic network interactions PLoS One 7 11 2012 e48927
52. K. Hu, F.A. Scheer, P. Ivanov, R.M. Buijs, and S.A. Shea The suprachiasmatic nucleus functions beyond circadian rhythm generation Neuroscience 149 3 2007 508 517
53. 2 + in single suprachiasmatic nucleus neurons Neuron 38 2 2003 253 263
54. S.T. Inouye, and H. Kawamura Persistence of circadian rhythmicity in a mammalian hypothalamic "island" containing the suprachiasmatic nucleus Proceedings of the National Academy of Sciences of the United States of America 76 11 1979 5962 5966
55. R.P. Irwin, and C.N. Allen Calcium response to retinohypothalamic tract synaptic transmission in suprachiasmatic nucleus neurons The Journal of Neuroscience 27 43 2007 11748 11757
56. R.P. Irwin, and C.N. Allen Neuropeptide-mediated calcium signaling in the suprachiasmatic nucleus network The European Journal of Neuroscience 32 9 2010 1497 1506
57. J. Itri, and C.S. Colwell Regulation of inhibitory synaptic transmission by vasoactive intestinal peptide (VIP) in the mouse suprachiasmatic nucleus Journal of Neurophysiology 90 3 2003 1589 1597
58. J.N. Itri, S. Michel, M.J. Vansteensel, J.H. Meijer, and C.S. Colwell Fast delayed rectifier potassium current is required for circadian neural activity Nature Neuroscience 8 5 2005 650 656
59. J.N. Itri, A.M. Vosko, A. Schroeder, J.M. Dragich, S. Michel, and C.S. Colwell Circadian regulation of a-type potassium currents in the suprachiasmatic nucleus Journal of Neurophysiology 103 2 2010 632 640
60. A.C. Jackson, G.L. Yao, and B.P. Bean Mechanism of spontaneous firing in dorsomedial suprachiasmatic nucleus neurons The Journal of Neuroscience 24 37 2004 7985 7998
61. A. Jagota, H.O. de la Iglesia, and W.J. Schwartz Morning and evening circadian oscillations in the suprachiasmatic nucleus in vitro Nature Neuroscience 3 4 2000 372 376
62. D.Y. Kim, H.J. Choi, J.S. Kim, Y.S. Kim, D.U. Jeong, and H.C. Shin Voltage-gated calcium channels play crucial roles in the glutamate-induced phase shifts of the rat suprachiasmatic circadian clock The European Journal of Neuroscience 21 5 2005 1215 1222
63. Y.I. Kim, and F.E. Dudek Intracellular electrophysiological study of suprachiasmatic nucleus neurons in rodents: Excitatory synaptic mechanisms The Journal of Physiology 444 1991 269 287
64. J.S. Kim, W.B. Kim, Y.B. Kim, Y. Lee, Y.S. Kim, and F.Y. Shen Chronic hyperosmotic stress converts GABAergic inhibition into excitation in vasopressin and oxytocin neurons in the rat The Journal of Neuroscience 31 37 2011 13312 13322
65. 2 +/calmodulin-dependent protein kinase II Neuron 29 1 2001 255 266
66. C.H. Ko, Y.R. Yamada, D.K. Welsh, E.D. Buhr, A.C. Liu, and E.E. Zhang Emergence of noise-induced oscillations in the central circadian pacemaker PLoS Biology 8 10 2010 e1000513
67. A. Kramer, F.C. Yang, P. Snodgrass, X. Li, T.E. Scammell, and F.C. Davis Regulation of daily locomotor activity and sleep by hypothalamic EGF receptor signaling Science 294 5551 2001 2511 2515
68. S. Kraves, and C.J. Weitz A role for cardiotrophin-like cytokine in the circadian control of mammalian locomotor activity Nature Neuroscience 9 2 2006 212 219
69. T. Kudo, D.H. Loh, D. Kuljis, C. Constance, and C.S. Colwell Fast delayed rectifier potassium current: Critical for input and output of the circadian system The Journal of Neuroscience 31 8 2011 2746 2755
70. S.J. Kuhlman, and D.G. McMahon Rhythmic regulation of membrane potential and potassium current persists in SCN neurons in the absence of environmental input The European Journal of Neuroscience 20 4 2004 1113 1117
71. R.K. Leak, J.P. Card, and R.Y. Moore Suprachiasmatic pacemaker organization analyzed by viral transynaptic transport Brain Research 819 1-2 1999 23 32
72. B. Li, W. Jie, L. Huang, P. Wei, S. Li, and Z. Luo Nuclear BK channels regulate gene expression via the control of nuclear calcium signaling Nature Neuroscience 17 8 2014 1055 1063
73. C. Liu, and S.M. Reppert GABA synchronizes clock cells within the suprachiasmatic circadian clock Neuron 25 1 2000 123 128
74. A.C. Liu, D.K. Welsh, C.H. Ko, H.G. Tran, E.E. Zhang, and A.A. Priest Intercellular coupling confers robustness against mutations in the SCN circadian clock network Cell 129 3 2007 605 616
75. D.H. Loh, J.M. Dragich, T. Kudo, A.M. Schroeder, T.J. Nakamura, and J.A. Waschek Effects of vasoactive intestinal peptide genotype on circadian gene expression in the suprachiasmatic nucleus and peripheral organs Journal of Biological Rhythms 26 3 2011 200 209
76. G.B. Lundkvist, Y. Kwak, E.K. Davis, H. Tei, and G.D. Block A calcium flux is required for circadian rhythm generation in mammalian pacemaker neurons The Journal of Neuroscience 25 33 2005 7682 7686
77. E.S. Maywood, J.E. Chesham, J.A. O'Brien, and M.H. Hastings A diversity of paracrine signals sustains molecular circadian cycling in suprachiasmatic nucleus circuits Proceedings of the National Academy of Sciences of the United States of America 108 34 2011 14306 14311
78. E.S. Maywood, A.B. Reddy, G.K. Wong, J.S. O'Neill, J.A. O'Brien, and D.G. McMahon Synchronization and maintenance of timekeeping in suprachiasmatic circadian clock cells by neuropeptidergic signaling Current Biology 16 6 2006 599 605
79. J.H. Meijer, S. Daan, G.J. Overkamp, and P.M. Hermann The two-oscillator circadian system of tree shrews (Tupaia belangeri) and its response to light and dark pulses Journal of Biological Rhythms 5 1 1990 1 16
80. J.H. Meijer, G.A. Groos, and B. Rusak Luminance coding in a circadian pacemaker: The suprachiasmatic nucleus of the rat and the hamster Brain Research 382 1 1986 109 118
81. J.H. Meijer, S. Michel, H.T. Vanderleest, and J.H. Rohling Daily and seasonal adaptation of the circadian clock requires plasticity of the SCN neuronal network The European Journal of Neuroscience 32 12 2010 2143 2151
82. J.H. Meijer, J. Schaap, K. Watanabe, and H. Albus Multiunit activity recordings in the suprachiasmatic nuclei: In vivo versus in vitro models Brain Research 753 2 1997 322 327
83. J.H. Meijer, K. Watanabe, J. Schaap, H. Albus, and L. Detari Light responsiveness of the suprachiasmatic nucleus: Long-term multiunit and single-unit recordings in freely moving rats The Journal of Neuroscience 18 21 1998 9078 9087
84. S. Michel, J. Itri, J.H. Han, K. Gniotczynski, and C.S. Colwell Regulation of glutamatergic signalling by PACAP in the mammalian suprachiasmatic nucleus BMC Neuroscience 7 2006 15
85. S. Michel, R. Marek, H.T. Vanderleest, M.J. Vansteensel, W.J. Schwartz, and C.S. Colwell Mechanism of bilateral communication in the suprachiasmatic nucleus The European Journal of Neuroscience 37 6 2013 964 971
86. R.Y. Moore, and V.B. Eichler Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat Brain Research 42 1 1972 201 206
87. R.Y. Moore, J.C. Speh, and R.K. Leak Suprachiasmatic nucleus organization Cell and Tissue Research 309 1 2002 89 98
88. L.P. Morin, and C.N. Allen The circadian visual system, 2005 Brain Research Reviews 51 1 2006 1 60
89. M. Mrugala, P. Zlomanczuk, A. Jagota, and W.J. Schwartz Rhythmic multiunit neural activity in slices of hamster suprachiasmatic nucleus reflect prior photoperiod American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 278 4 2000 R987 R994
90. N.I. Muraro, N. Pirez, and M.F. Ceriani The circadian system: Plasticity at many levels Neuroscience 247 2013 280 293
91. M. Nagano, A. Adachi, K. Nakahama, T. Nakamura, M. Tamada, and E. Meyer-Bernstein An abrupt shift in the day/night cycle causes desynchrony in the mammalian circadian center The Journal of Neuroscience 23 14 2003 6141 6151
92. S.S. Nahm, Y.Z. Farnell, W. Griffith, and D.J. Earnest Circadian regulation and function of voltage-dependent calcium channels in the suprachiasmatic nucleus The Journal of Neuroscience 25 40 2005 9304 9308
93. E. Naito, T. Watanabe, H. Tei, T. Yoshimura, and S. Ebihara Reorganization of the suprachiasmatic nucleus coding for day length Journal of Biological Rhythms 23 2 2008 140 149
94. T.J. Nakamura, K. Fujimura, S. Ebihara, and K. Shinohara Light response of the neuronal firing activity in the suprachiasmatic nucleus of mice Neuroscience Letters 371 2-3 2004 244 248
95. W. Nakamura, S. Honma, T. Shirakawa, and K. Honma Regional pacemakers composed of multiple oscillator neurons in the rat suprachiasmatic nucleus The European Journal of Neuroscience 14 4 2001 666 674
96. W. Nakamura, S. Yamazaki, N.N. Takasu, K. Mishima, and G.D. Block Differential response of Period 1 expression within the suprachiasmatic nucleus The Journal of Neuroscience 25 23 2005 5481 5487
97. M.N. Nitabach, J. Blau, and T.C. Holmes Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock Cell 109 4 2002 485 495
98. H. Ohta, S. Yamazaki, and D.G. McMahon Constant light desynchronizes mammalian clock neurons Nature Neuroscience 8 3 2005 267 269
99. J.S. O'Neill, E.S. Maywood, J.E. Chesham, J.S. Takahashi, and M.H. Hastings cAMP-dependent signaling as a core component of the mammalian circadian pacemaker Science 320 5878 2008 949 953
100. M. Palomba, M. Nygard, F. Florenzano, G. Bertini, K. Kristensson, and M. Bentivoglio Decline of the presynaptic network, including GABAergic terminals, in the aging suprachiasmatic nucleus of the mouse Journal of Biological Rhythms 23 3 2008 220 231
101. S. Panda, M.P. Antoch, B.H. Miller, A.I. Su, A.B. Schook, and M. Straume Coordinated transcription of key pathways in the mouse by the circadian clock Cell 109 3 2002 307 320
102. S. Panda, I. Provencio, D.C. Tu, S.S. Pires, M.D. Rollag, and A.M. Castrucci Melanopsin is required for non-image-forming photic responses in blind mice Science 301 5632 2003 525 527
103. C.M. Pennartz, M.T. de Jeu, N.P. Bos, J. Schaap, and A.M. Geurtsen Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock Nature 416 6878 2002 286 290
104. C.S. Pittendrigh, and S. Daan A functional analysis of circadian pacemakers in nocturnal rodents. V. Pacemaker structure: A clock for all seasons Journal of Computational Physiology 106 3 1976 333 355
105. G. Rey, and A.B. Reddy Connecting cellular metabolism to circadian clocks Trends in Cell Biology 23 5 2013 234 241
106. J.H. Rohling, H.T. vanderLeest, S. Michel, M.J. Vansteensel, and J.H. Meijer Phase resetting of the mammalian circadian clock relies on a rapid shift of a small population of pacemaker neurons PLoS One 6 9 2011 e25437
107. H.J. Romijn, A.A. Sluiter, C.W. Pool, J. Wortel, and R.M. Buijs Evidence from confocal fluorescence microscopy for a dense, reciprocal innervation between AVP-, somatostatin-, VIP/PHI-, GRP-, and VIP/PHI/GRP-immunoreactive neurons in the rat suprachiasmatic nucleus The European Journal of Neuroscience 9 12 1997 2613 2623
108. N.F. Ruby, T.J. Brennan, X.M. Xie, V. Cao, P. Franken, and H.C. Heller Role of melanopsin in circadian responses to light Science 298 5601 2002 2211 2213
109. N.F. Ruby, D.E. Burns, and H.C. Heller Circadian rhythms in the suprachiasmatic nucleus are temperature-compensated and phase-shifted by heat pulses in vitro The Journal of Neuroscience 19 19 1999 8630 8636
110. J. Schaap, H. Albus, H.T. VanderLeest, P.H. Eilers, L. Detari, and J.H. Meijer Heterogeneity of rhythmic suprachiasmatic nucleus neurons: Implications for circadian waveform and photoperiodic encoding Proceedings of the National Academy of Sciences of the United States of America 100 26 2003 15994 15999
111. J. Schaap, N.P. Bos, M.T. de Jeu, A.M. Geurtsen, J.H. Meijer, and C.M. Pennartz Neurons of the rat suprachiasmatic nucleus show a circadian rhythm in membrane properties that is lost during prolonged whole-cell recording Brain Research 815 1 1999 154 166
112. J. Schaap, and J.H. Meijer Opposing effects of behavioural activity and light on neurons of the suprachiasmatic nucleus The European Journal of Neuroscience 13 10 2001 1955 1962
113. W.J. Schwartz, R.A. Gross, and M.T. Morton The suprachiasmatic nuclei contain a tetrodotoxin-resistant circadian pacemaker Proceedings of the National Academy of Sciences of the United States of America 84 6 1987 1694 1698
114. S. Shibata, Y. Oomura, H. Kita, and K. Hattori Circadian rhythmic changes of neuronal activity in the suprachiasmatic nucleus of the rat hypothalamic slice Brain Research 247 1 1982 154 158
115. K. Shinohara, S. Honma, Y. Katsuno, H. Abe, and K. Honma Circadian release of amino acids in the suprachiasmatic nucleus in vitro Neuroreport 9 1 1998 137 140
116. M.M. Sidor, and C.A. McClung Timing matters: Using optogenetics to chronically manipulate neural circuitry and rhythms Frontiers in Behavioral Neuroscience 8 2014 41
117. R. Silver, J. LeSauter, P.A. Tresco, and M.N. Lehman A diffusible coupling signal from the transplanted suprachiasmatic nucleus controlling circadian locomotor rhythms Nature 382 6594 1996 810 813
118. F.K. Stephan, and I. Zucker Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions Proceedings of the National Academy of Sciences of the United States of America 69 6 1972 1583 1586
119. X. Sun, S. Whitefield, B. Rusak, and K. Semba Electrophysiological analysis of suprachiasmatic nucleus projections to the ventrolateral preoptic area in the rat The European Journal of Neuroscience 14 8 2001 1257 1274
120. L. Tian, S.A. Hires, T. Mao, D. Huber, M.E. Chiappe, and S.H. Chalasani Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators Nature Methods 6 12 2009 875 881
121. H.C. van Diepen, A. Ramkisoensing, S.N. Peirson, R.G. Foster, and J.H. Meijer Irradiance encoding in the suprachiasmatic nuclei by rod and cone photoreceptors FASEB Journal 27 10 2013 4204 4212
122. F. van Oosterhout, S.P. Fisher, H.C. van Diepen, T.S. Watson, T. Houben, and H.T. VanderLeest Ultraviolet light provides a major input to non-image-forming light detection in mice Current Biology 22 15 2012 1397 1402
123. F. van Oosterhout, E.A. Lucassen, T. Houben, H.T. vanderLeest, M.C. Antle, and J.H. Meijer Amplitude of the SCN clock enhanced by the behavioral activity rhythm PLoS One 7 6 2012 e39693
124. H.T. VanderLeest, T. Houben, S. Michel, T. Deboer, H. Albus, and M.J. Vansteensel Seasonal encoding by the circadian pacemaker of the SCN Current Biology 17 5 2007 468 473
125. H.T. vanderLeest, M.J. Vansteensel, H. Duindam, S. Michel, and J.H. Meijer Phase of the electrical activity rhythm in the SCN in vitro not influenced by preparation time Chronobiology International 26 6 2009 1075 1089
126. T.A. Wang, Y.V. Yu, G. Govindaiah, X. Ye, L. Artinian, and T.P. Coleman Circadian rhythm of redox state regulates excitability in suprachiasmatic nucleus neurons Science 337 6096 2012 839 842
127. A.B. Webb, N. Angelo, J.E. Huettner, and E.D. Herzog Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons Proceedings of the National Academy of Sciences of the United States of America 106 38 2009 16493 16498
128. D.K. Welsh, D.E. Logothetis, M. Meister, and S.M. Reppert Individual neurons dissociated from rat suprachiasmatic nucleus express independently phased circadian firing rhythms Neuron 14 4 1995 697 706
129. D.K. Welsh, J.S. Takahashi, and S.A. Kay Suprachiasmatic nucleus: Cell autonomy and network properties Annual Review of Physiology 72 2010 551 577
130. M. Whitaker Genetically encoded probes for measurement of intracellular calcium Methods in Cell Biology 99 2010 153 182
131. S. Yamaguchi, H. Isejima, T. Matsuo, R. Okura, K. Yagita, and M. Kobayashi Synchronization of cellular clocks in the suprachiasmatic nucleus Science 302 5649 2003 1408 1412
132. S. Yamazaki, M.C. Kerbeshian, C.G. Hocker, G.D. Block, and M. Menaker Rhythmic properties of the hamster suprachiasmatic nucleus in vivo The Journal of Neuroscience 18 24 1998 10709 10723
133. S. Yamazaki, R. Numano, M. Abe, A. Hida, R. Takahashi, and M. Ueda Resetting central and peripheral circadian oscillators in transgenic rats Science 288 5466 2000 682 685
134. L. Yan, and R. Silver Resetting the brain clock: Time course and localization of mPER1 and mPER2 protein expression in suprachiasmatic nuclei during phase shifts The European Journal of Neuroscience 19 4 2004 1105 1109
135. J.N. Zhou, M.A. Hofman, and D.F. Swaab VIP neurons in the human SCN in relation to sex, age, and Alzheimer's disease Neurobiology of Aging 16 4 1995 571 576