Circadian rhythms and memory formation (original) (raw)

References

1. Folkard, S., Wever, R. A. & Wildgruber, C. M. Multi-oscillatory control of circadian rhythms in human performance. Nature 305, 223–226 (1983).
   CAS PubMed Google Scholar
2. Monk, T. H. et al. Task variables determine which biological clock controls circadian rhythms in human performance. Nature 304, 543–545 (1983).
   CAS PubMed Google Scholar
3. Monk, T. H., Weitzman, E. D., Fookson, J. E. & Moline, M. L. Circadian rhythms in human performance efficiency under free-running conditions. Chronobiologia 11, 343–354 (1984).
   CAS PubMed Google Scholar
4. Davies, J. A., Navaratnam, V. & Redfern, P. H. A 24-hour rhythm in passive-avoidance behaviour in rats. Psychopharmacologia 32, 211–214 (1973).
   CAS PubMed Google Scholar
5. Holloway, F. A. & Wansley, R. A. Multiple retention deficits at periodic intervals after active and passive avoidance learning. Behav. Biol. 9, 1–14 (1973).
   CAS PubMed Google Scholar
6. Tapp, W. N. & Holloway, F. A. Phase shifting circadian rhythms produces retrograde amnesia. Science 211, 1056–1058 (1981).
   CAS PubMed Google Scholar
7. Fekete, M., van Ree, J. M., Niesink, R. J. & de Wied, D. Disrupting circadian rhythms in rats induces retrograde amnesia. Physiol. Behav. 34, 883–887 (1985).
   CAS PubMed Google Scholar
8. Gerstner, J. R. et al. Cycling behavior and memory formation. J. Neurosci. 29, 12824–12830 (2009).
   CAS PubMed PubMed Central Google Scholar
9. Takahashi, J. S., Hong, H. K., Ko, C. H. & McDearmon, E. L. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nature Rev. Genet. 9, 764–775 (2008).
   CAS PubMed Google Scholar
10. Herzog, E. D. Neurons and networks in daily rhythms. Nature Rev. Neurosci. 8, 790–802 (2007).
    CAS Google Scholar
11. Kandel, E. R. The biology of memory: a forty-year perspective. J. Neurosci. 29, 12748–12756 (2009).
    CAS PubMed PubMed Central Google Scholar
12. Silva, A. J., Zhou, Y., Rogerson, T., Shobe, J. & Balaji, J. Molecular and cellular approaches to memory allocation in neural circuits. Science 326, 391–395 (2009).
    CAS PubMed PubMed Central Google Scholar
13. Konopka, R. J. & Benzer, S. Clock mutants of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 68, 2112–2116 (1971).
    CAS PubMed PubMed Central Google Scholar
14. Bargiello, T. A., Jackson, F. R. & Young, M. W. Restoration of circadian behavioural rhythms by gene transfer in Drosophila. Nature 312, 752–754 (1984).
    CAS PubMed Google Scholar
15. Reddy, P. et al. Molecular analysis of the period locus in Drosophila melanogaster and identification of a transcript involved in biological rhythms. Cell 38, 701–710 (1984).
    CAS PubMed Google Scholar
16. Panda, S., Hogenesch, J. B. & Kay, S. A. Circadian rhythms from flies to human. Nature 417, 329–335 (2002).
    CAS PubMed Google Scholar
17. Gallego, M. & Virshup, D. M. Post-translational modifications regulate the ticking of the circadian clock. Nature Rev. Mol. Cell Biol. 8, 139–148 (2007).
    CAS Google Scholar
18. Lyons, L. C., Green, C. L. & Eskin, A. Intermediate-term memory is modulated by the circadian clock. J. Biol. Rhythms 23, 538–542 (2008).
    PubMed PubMed Central Google Scholar
19. Sakai, T., Tamura, T., Kitamoto, T. & Kidokoro, Y. A clock gene, period, plays a key role in long-term memory formation in Drosophila. Proc. Natl Acad. Sci. USA 101, 16058–16063 (2004). This study implicates a core clock gene in the regulation of LTM, reinforcing the pleiotropic nature of circadian genes in multiple behaviours, including memory.
    CAS PubMed PubMed Central Google Scholar
20. Belvin, M. P., Zhou, H. & Yin, J. C. The Drosophila dCREB2 gene affects the circadian clock. Neuron 22, 777–787 (1999).
    CAS PubMed Google Scholar
21. O'Neill, J. S., Maywood, E. S., Chesham, J. E., Takahashi, J. S. & Hastings, M. H. cAMP-dependent signaling as a core component of the mammalian circadian pacemaker. Science 320, 949–953 (2008).
    CAS PubMed PubMed Central Google Scholar
22. Travnickova-Bendova, Z., Cermakian, N., Reppert, S. M. & Sassone-Corsi, P. Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity. Proc. Natl Acad. Sci. USA 99, 7728–7733 (2002).
    CAS PubMed PubMed Central Google Scholar
23. Antle, M. C. & Silver, R. Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci. 28, 145–151 (2005).
    CAS PubMed Google Scholar
24. Hankins, M. W., Peirson, S. N. & Foster, R. G. Melanopsin: an exciting photopigment. Trends Neurosci. 31, 27–36 (2008).
    CAS PubMed Google Scholar
25. Peng, Z. C. & Bentivoglio, M. The thalamic paraventricular nucleus relays information from the suprachiasmatic nucleus to the amygdala: a combined anterograde and retrograde tracing study in the rat at the light and electron microscopic levels. J. Neurocytol. 33, 101–116 (2004).
    CAS PubMed Google Scholar
26. Moga, M. M., Weis, R. P. & Moore, R. Y. Efferent projections of the paraventricular thalamic nucleus in the rat. J. Comp. Neurol. 359, 221–238 (1995).
    CAS PubMed Google Scholar
27. Peyron, C. et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J. Neurosci. 18, 9996–10015 (1998).
    CAS PubMed PubMed Central Google Scholar
28. Perreau-Lenz, S. et al. Suprachiasmatic control of melatonin synthesis in rats: inhibitory and stimulatory mechanisms. Eur. J. Neurosci. 17, 221–228 (2003).
    PubMed Google Scholar
29. Ashmore, L. J. & Sehgal, A. A fly's eye view of circadian entrainment. J. Biol. Rhythms 18, 206–216 (2003).
    PubMed Google Scholar
30. Stanewsky, R. et al. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681–692 (1998).
    CAS PubMed Google Scholar
31. Veleri, S., Rieger, D., Helfrich-Forster, C. & Stanewsky, R. Hofbauer-Buchner eyelet affects circadian photosensitivity and coordinates TIM and PER expression in Drosophila clock neurons. J. Biol. Rhythms 22, 29–42 (2007).
    PubMed Google Scholar
32. Veleri, S., Brandes, C., Helfrich-Forster, C., Hall, J. C. & Stanewsky, R. A self-sustaining, light-entrainable circadian oscillator in the Drosophila brain. Curr. Biol. 13, 1758–1767 (2003).
    CAS PubMed Google Scholar
33. Helfrich-Forster, C., Winter, C., Hofbauer, A., Hall, J. C. & Stanewsky, R. The circadian clock of fruit flies is blind after elimination of all known photoreceptors. Neuron 30, 249–261 (2001).
    CAS PubMed Google Scholar
34. Emery, P., So, W. V., Kaneko, M., Hall, J. C. & Rosbash, M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95, 669–679 (1998).
    CAS PubMed Google Scholar
35. Kaneko, M. & Hall, J. C. Neuroanatomy of cells expressing clock genes in Drosophila: transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J. Comp. Neurol. 422, 66–94 (2000).
    CAS PubMed Google Scholar
36. Cao, G. & Nitabach, M. N. Circadian control of membrane excitability in Drosophila melanogaster lateral ventral clock neurons. J. Neurosci. 28, 6493–6501 (2008).
    CAS PubMed PubMed Central Google Scholar
37. Yasuyama, K. & Meinertzhagen, I. A. Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster. J. Comp. Neurol. 412, 193–202 (1999).
    CAS PubMed Google Scholar
38. Helfrich-Forster, C. et al. The extraretinal eyelet of Drosophila: development, ultrastructure, and putative circadian function. J. Neurosci. 22, 9255–9266 (2002).
    PubMed PubMed Central Google Scholar
39. Malpel, S., Klarsfeld, A. & Rouyer, F. Larval optic nerve and adult extra-retinal photoreceptors sequentially associate with clock neurons during Drosophila brain development. Development 129, 1443–1453 (2002).
    CAS PubMed Google Scholar
40. Pitman, J. L., McGill, J. J., Keegan, K. P. & Allada, R. A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 441, 753–756 (2006).
    CAS PubMed Google Scholar
41. Joiner, W. J., Crocker, A., White, B. H. & Sehgal, A. Sleep in Drosophila is regulated by adult mushroom bodies. Nature 441, 757–760 (2006).
    CAS PubMed Google Scholar
42. McBride, S. M. et al. Mushroom body ablation impairs short-term memory and long-term memory of courtship conditioning in Drosophila melanogaster. Neuron 24, 967–977 (1999).
    CAS PubMed Google Scholar
43. Pascual, A. & Preat, T. Localization of long-term memory within the Drosophila mushroom body. Science 294, 1115–1117 (2001).
    CAS PubMed Google Scholar
44. Helfrich-Forster, C. The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 92, 612–616 (1995).
    CAS PubMed PubMed Central Google Scholar
45. Green, D. J. & Gillette, R. Circadian rhythm of firing rate recorded from single cells in the rat suprachiasmatic brain slice. Brain Res. 245, 198–200 (1982).
    CAS PubMed Google Scholar
46. Groos, G. & Hendriks, J. Circadian rhythms in electrical discharge of rat suprachiasmatic neurones recorded in vitro. Neurosci. Lett. 34, 283–288 (1982).
    CAS PubMed Google Scholar
47. de Jeu, M., Hermes, M. & Pennartz, C. Circadian modulation of membrane properties in slices of rat suprachiasmatic nucleus. Neuroreport 9, 3725–3729 (1998).
    CAS PubMed Google Scholar
48. Kuhlman, S. J. & McMahon, D. G. Rhythmic regulation of membrane potential and potassium current persists in SCN neurons in the absence of environmental input. Eur. J. Neurosci. 20, 1113–1117 (2004).
    PubMed Google Scholar
49. Pennartz, C. M., de Jeu, M. T., Bos, N. P., Schaap, J. & Geurtsen, A. M. Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock. Nature 416, 286–290 (2002).
    CAS PubMed Google Scholar
50. Kononenko, N. I., Kuehl-Kovarik, M. C., Partin, K. M. & Dudek, F. E. Circadian difference in firing rate of isolated rat suprachiasmatic nucleus neurons. Neurosci. Lett. 436, 314–316 (2008).
    CAS PubMed Google Scholar
51. Park, D. & Griffith, L. C. Electrophysiological and anatomical characterization of PDF-positive clock neurons in the intact adult Drosophila brain. J. Neurophysiol. 95, 3955–3960 (2006).
    PubMed Google Scholar
52. Sheeba, V., Gu, H., Sharma, V. K., O'Dowd, D. K. & Holmes, T. C. Circadian- and light-dependent regulation of resting membrane potential and spontaneous action potential firing of Drosophila circadian pacemaker neurons. J. Neurophysiol. 99, 976–988 (2008).
    PubMed Google Scholar
53. Pandi-Perumal, S. R. et al. Melatonin: nature's most versatile biological signal? FEBS J. 273, 2813–2838 (2006).
    CAS PubMed Google Scholar
54. Shimomura, K. et al. Genetic suppression of the circadian Clock mutation by the melatonin biosynthesis pathway. Proc. Natl Acad. Sci. USA 107, 8399–8403 (2010).
    CAS PubMed PubMed Central Google Scholar
55. Benloucif, S. et al. Stability of melatonin and temperature as circadian phase markers and their relation to sleep times in humans. J. Biol. Rhythms 20, 178–188 (2005).
    CAS PubMed Google Scholar
56. Cahill, G. M. Circadian regulation of melatonin production in cultured zebrafish pineal and retina. Brain Res. 708, 177–181 (1996).
    CAS PubMed Google Scholar
57. Abran, D., Anctil, M. & Ali, M. A. Melatonin activity rhythms in eyes and cerebral ganglia of Aplysia californica. Gen. Comp. Endocrinol. 96, 215–222 (1994).
    CAS PubMed Google Scholar
58. Goto, M., Oshima, I., Tomita, T. & Ebihara, S. Melatonin content of the pineal gland in different mouse strains. J. Pineal Res. 7, 195–204 (1989).
    CAS PubMed Google Scholar
59. Hintermann, E., Grieder, N. C., Amherd, R., Brodbeck, D. & Meyer, U. A. Cloning of an arylalkylamine N-acetyltransferase (aaNAT1) from Drosophila melanogaster expressed in the nervous system and the gut. Proc. Natl Acad. Sci. USA 93, 12315–12320 (1996).
    CAS PubMed PubMed Central Google Scholar
60. McArthur, A. J., Gillette, M. U. & Prosser, R. A. Melatonin directly resets the rat suprachiasmatic circadian clock in vitro. Brain Res. 565, 158–161 (1991).
    CAS PubMed Google Scholar
61. Rusak, B. & Yu, G. D. Regulation of melatonin-sensitivity and firing-rate rhythms of hamster suprachiasmatic nucleus neurons: pinealectomy effects. Brain Res. 602, 200–204 (1993).
    CAS PubMed Google Scholar
62. Starkey, S. J., Walker, M. P., Beresford, I. J. & Hagan, R. M. Modulation of the rat suprachiasmatic circadian clock by melatonin in vitro. Neuroreport 6, 1947–1951 (1995).
    CAS PubMed Google Scholar
63. Musshoff, U., Riewenherm, D., Berger, E., Fauteck, J. D. & Speckmann, E. J. Melatonin receptors in rat hippocampus: molecular and functional investigations. Hippocampus 12, 165–173 (2002).
    CAS PubMed Google Scholar
64. Martin, S. J., Grimwood, P. D. & Morris, R. G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649–711 (2000).
    CAS PubMed Google Scholar
65. Barnes, C. A., McNaughton, B. L., Goddard, G. V., Douglas, R. M. & Adamec, R. Circadian rhythm of synaptic excitability in rat and monkey central nervous system. Science 197, 91–92 (1977).
    CAS PubMed Google Scholar
66. West, M. O. & Deadwyler, S. A. Circadian modulation of granule cell response to perforant path synaptic input in the rat. Neuroscience 5, 1597–1602 (1980).
    CAS PubMed Google Scholar
67. Harris, K. M. & Teyler, T. J. Age differences in a circadian influence on hippocampal LTP. Brain Res. 261, 69–73 (1983).
    CAS PubMed Google Scholar
68. Dana, R. C. & Martinez, J. L. Jr. Effect of adrenalectomy on the circadian rhythm of LTP. Brain Res. 308, 392–395 (1984).
    CAS PubMed Google Scholar
69. Nishikawa, Y., Shibata, S. & Watanabe, S. Circadian changes in long-term potentiation of rat suprachiasmatic field potentials elicited by optic nerve stimulation in vitro. Brain Res. 695, 158–162 (1995).
    CAS PubMed Google Scholar
70. Chaudhury, D., Wang, L. M. & Colwell, C. S. Circadian regulation of hippocampal long-term potentiation. J. Biol. Rhythms 20, 225–236 (2005).
    PubMed PubMed Central Google Scholar
71. Abraham, W. C. & Bear, M. F. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19, 126–130 (1996).
    CAS PubMed Google Scholar
72. Whitlock, J. R., Heynen, A. J., Shuler, M. G. & Bear, M. F. Learning induces long-term potentiation in the hippocampus. Science 313, 1093–1097 (2006).
    CAS PubMed Google Scholar
73. Raghavan, A. V., Horowitz, J. M. & Fuller, C. A. Diurnal modulation of long-term potentiation in the hamster hippocampal slice. Brain Res. 833, 311–314 (1999).
    CAS PubMed Google Scholar
74. Fukunaga, K., Horikawa, K., Shibata, S., Takeuchi, Y. & Miyamoto, E. Ca2+/calmodulin-dependent protein kinase II-dependent long-term potentiation in the rat suprachiasmatic nucleus and its inhibition by melatonin. J. Neurosci. Res. 70, 799–807 (2002).
    CAS PubMed Google Scholar
75. Collins, D. R. & Davies, S. N. Melatonin blocks the induction of long-term potentiation in an N-methyl-D-aspartate independent manner. Brain Res. 767, 162–165 (1997).
    CAS PubMed Google Scholar
76. Wang, L. M., Suthana, N. A., Chaudhury, D., Weaver, D. R. & Colwell, C. S. Melatonin inhibits hippocampal long-term potentiation. Eur. J. Neurosci. 22, 2231–2237 (2005).
    PubMed PubMed Central Google Scholar
77. Ozcan, M., Yilmaz, B. & Carpenter, D. O. Effects of melatonin on synaptic transmission and long-term potentiation in two areas of mouse hippocampus. Brain Res. 1111, 90–94 (2006).
    CAS PubMed Google Scholar
78. Soto-Moyano, R. et al. Melatonin administration impairs visuo-spatial performance and inhibits neocortical long-term potentiation in rats. Pharmacol. Biochem. Behav. 85, 408–414 (2006).
    CAS PubMed Google Scholar
79. Rawashdeh, O., de Borsetti, N. H., Roman, G. & Cahill, G. M. Melatonin suppresses nighttime memory formation in zebrafish. Science 318, 1144–1146 (2007). This study describes a time-of-day effect on memory formation in zebrafish, and shows that the hormone melatonin is necessary for the night-time suppression of memory.
    CAS PubMed Google Scholar
80. Moore, R. Y. & Eichler, V. B. Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res. 42, 201–206 (1972).
    CAS PubMed Google Scholar
81. Valentinuzzi, V. S. & Ferrari, E. A. Habituation to sound during morning and night sessions in pigeons (Columba livia). Physiol. Behav. 62, 1203–1209 (1997).
    CAS PubMed Google Scholar
82. Valentinuzzi, V. S., Menna-Barreto, L. & Xavier, G. F. Effect of circadian phase on performance of rats in the Morris water maze task. J. Biol. Rhythms 19, 312–324 (2004).
    PubMed Google Scholar
83. Valentinuzzi, V. S. et al. Memory for time of training modulates performance on a place conditioning task in marmosets. Neurobiol. Learn. Mem. 89, 604–607 (2008).
    CAS PubMed Google Scholar
84. Moura, P. J., Gimenes-Junior, J. A., Valentinuzzi, V. S. & Xavier, G. F. Circadian phase and intertrial interval interfere with social recognition memory. Physiol. Behav. 96, 51–56 (2009).
    CAS PubMed Google Scholar
85. Walker, M. P. & Stickgold, R. Sleep, memory, and plasticity. Annu. Rev. Psychol. 57, 139–166 (2006).
    PubMed Google Scholar
86. Frank, M. G. & Benington, J. H. The role of sleep in memory consolidation and brain plasticity: dream or reality? Neuroscientist 12, 477–488 (2006).
    PubMed Google Scholar
87. Diekelmann, S. & Born, J. The memory function of sleep. Nature Rev. Neurosci. 11, 114–126 (2010).
    CAS Google Scholar
88. Fernandez, R. I., Lyons, L. C., Levenson, J., Khabour, O. & Eskin, A. Circadian modulation of long-term sensitization in Aplysia. Proc. Natl Acad. Sci. USA 100, 14415–14420 (2003). This paper describes the circadian control of a form of non-associative learning observed in sea slugs, which suggests that the circadian effects on memory processes are evolutionarily conserved.
    CAS PubMed PubMed Central Google Scholar
89. Chaudhury, D. & Colwell, C. S. Circadian modulation of learning and memory in fear-conditioned mice. Behav. Brain Res. 133, 95–108 (2002). This paper describes in extensive detail, that both hippocampal and amygdala-dependent memory follow a circadian rhythm.
    PubMed Google Scholar
90. Lyons, L. C. & Roman, G. Circadian modulation of short-term memory in Drosophila. Learn. Mem. 16, 19–27 (2008). This study describes a time-of-day effect on olfactory avoidance-conditioning, and shows that this rhythm can be blocked by arrhythmic behaviour resulting from either clock mutants or constant lighting conditions.
    PubMed Google Scholar
91. Wright, K. P. Jr, Hull, J. T., Hughes, R. J., Ronda, J. M. & Czeisler, C. A. Sleep and wakefulness out of phase with internal biological time impairs learning in humans. J. Cogn. Neurosci. 18, 508–521 (2006).
    PubMed Google Scholar
92. Roseboom, P. H. et al. Natural melatonin 'knockdown' in C57BL/6J mice: rare mechanism truncates serotonin N-acetyltransferase. Brain Res. Mol. Brain Res. 63, 189–197 (1998).
    CAS PubMed Google Scholar
93. Ebihara, S., Marks, T., Hudson, D. J. & Menaker, M. Genetic control of melatonin synthesis in the pineal gland of the mouse. Science 231, 491–493 (1986).
    CAS PubMed Google Scholar
94. Decker, S., McConnaughey, S. & Page, T. L. Circadian regulation of insect olfactory learning. Proc. Natl Acad. Sci. USA 104, 15905–15910 (2007).
    CAS PubMed PubMed Central Google Scholar
95. Lyons, L. C., Rawashdeh, O., Katzoff, A., Susswein, A. J. & Eskin, A. Circadian modulation of complex learning in diurnal and nocturnal Aplysia. Proc. Natl Acad. Sci. USA 102, 12589–12594 (2005).
    CAS PubMed PubMed Central Google Scholar
96. Eckel-Mahan, K. L. et al. Circadian oscillation of hippocampal MAPK activity and cAMP: implications for memory persistence. Nature Neurosci. 11, 1074–1082 (2008). This paper describes the pinnacle finding that the persistence of hippocampus-dependent memory relies on the circadian cycling of specific molecules.
    CAS PubMed Google Scholar
97. Kandel, E. R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030–1038 (2001).
    CAS PubMed Google Scholar
98. Yin, J. C. et al. Induction of a dominant negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79, 49–58 (1994).
    CAS PubMed Google Scholar
99. Yin, J. C., Del Vecchio, M., Zhou, H. & Tully, T. CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81, 107–115 (1995).
    CAS PubMed Google Scholar
100. Gonzales, E. D. et al. dCREB2-mediated enhancement of memory formation. Soc. Neurosci. Abstr. 35, 497.7, 3–4 (2009).
     Google Scholar
101. Lyons, L. C., Collado, M. S., Khabour, O., Green, C. L. & Eskin, A. The circadian clock modulates core steps in long-term memory formation in Aplysia. J. Neurosci. 26, 8662–8671 (2006).
     CAS PubMed PubMed Central Google Scholar
102. Borrelli, E., Nestler, E. J., Allis, C. D. & Sassone-Corsi, P. Decoding the epigenetic language of neuronal plasticity. Neuron 60, 961–974 (2008).
     CAS PubMed PubMed Central Google Scholar
103. Crosio, C., Heitz, E., Allis, C. D., Borrelli, E. & Sassone-Corsi, P. Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. J. Cell Sci. 116, 4905–4914 (2003).
     CAS PubMed Google Scholar
104. Crosio, C., Cermakian, N., Allis, C. D. & Sassone-Corsi, P. Light induces chromatin modification in cells of the mammalian circadian clock. Nature Neurosci. 3, 1241–1247 (2000).
     CAS PubMed Google Scholar
105. Etchegaray, J. P., Lee, C., Wade, P. A. & Reppert, S. M. Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature 421, 177–182 (2003).
     CAS PubMed Google Scholar
106. Naruse, Y. et al. Circadian and light-induced transcription of clock gene Per1 depends on histone acetylation and deacetylation. Mol. Cell. Biol. 24, 6278–6287 (2004).
     CAS PubMed PubMed Central Google Scholar
107. Ripperger, J. A. & Schibler, U. Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nature Genet. 38, 369–374 (2006).
     CAS PubMed Google Scholar
108. Doi, M., Hirayama, J. & Sassone-Corsi, P. Circadian regulator CLOCK is a histone acetyltransferase. Cell 125, 497–508 (2006).
     CAS PubMed Google Scholar
109. Kondratova, A. A., Dubrovsky, Y. V., Antoch, M. P. & Kondratov, R. V. Circadian clock proteins control adaptation to novel environment and memory formation. Aging (Albany, N.Y.) 2, 285–297 (2010). Using the open field paradigm in mice, this study describes circadian molecules as regulators of LTM formation, providing evidence of core clock components for memory processing in mammals.
     CAS Google Scholar
110. Levenson, J. M. et al. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 279, 40545–40559 (2004).
     CAS PubMed Google Scholar
111. Levenson, J. M. & Sweatt, J. D. Epigenetic mechanisms in memory formation. Nature Rev. Neurosci. 6, 108–118 (2005).
     CAS Google Scholar
112. Lamont, E. W., Robinson, B., Stewart, J. & Amir, S. The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc. Natl Acad. Sci. USA 102, 4180–4184 (2005).
     CAS PubMed PubMed Central Google Scholar
113. Cain, S. W. & Ralph, M. R. Circadian modulation of conditioned place avoidance in hamsters does not require the suprachiasmatic nucleus. Neurobiol. Learn. Mem. 91, 81–84 (2009).
     PubMed Google Scholar
114. Garcia, J. A. et al. Impaired cued and contextual memory in NPAS2-deficient mice. Science 288, 2226–2230 (2000).
     CAS PubMed Google Scholar
115. Van der Zee, E. A. et al. Circadian time-place learning in mice depends on Cry genes. Curr. Biol. 18, 844–848 (2008). Using a novel time–place learning paradigm, this study describes cryptochrome genes as being necessary for proper time–place associations, and provides evidence for the molecular clock in time-stamp memory.
     CAS PubMed Google Scholar
116. Holloway, F. A. & Wansley, R. Multiphasic retention deficits at periodic intervals after passive-avoidance learning. Science 180, 208–210 (1973).
     CAS PubMed Google Scholar
117. Stephan, F. K. & Kovacevic, N. S. Multiple retention deficit in passive avoidance in rats is eliminated by suprachiasmatic lesions. Behav. Biol. 22, 456–462 (1978).
     CAS PubMed Google Scholar
118. McBride, S. M. et al. Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of fragile X syndrome. Neuron 45, 753–764 (2005).
     CAS PubMed Google Scholar
119. Bolduc, F. V., Bell, K., Cox, H., Broadie, K. S. & Tully, T. Excess protein synthesis in Drosophila fragile X mutants impairs long-term memory. Nature Neurosci. 11, 1143–1145 (2008).
     CAS PubMed Google Scholar
120. Dockendorff, T. C. et al. Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron 34, 973–984 (2002).
     CAS PubMed Google Scholar
121. Inoue, S. et al. A role for the Drosophila fragile X-related gene in circadian output. Curr. Biol. 12, 1331–1335 (2002).
     CAS PubMed Google Scholar
122. Gu, Y. et al. Impaired conditioned fear and enhanced long-term potentiation in Fmr2 knock-out mice. J. Neurosci. 22, 2753–2763 (2002).
     CAS PubMed PubMed Central Google Scholar
123. Zhao, M. G. et al. Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. J. Neurosci. 25, 7385–7392 (2005).
     CAS PubMed PubMed Central Google Scholar
124. Zhang, J. et al. Fragile X-related proteins regulate mammalian circadian behavioral rhythms. Am. J. Hum. Genet. 83, 43–52 (2008).
     CAS PubMed PubMed Central Google Scholar
125. Vosko, A. M., Schroeder, A., Loh, D. H. & Colwell, C. S. Vasoactive intestinal peptide and the mammalian circadian system. Gen. Comp. Endocrinol. 152, 165–175 (2007).
     CAS PubMed PubMed Central Google Scholar
126. Chaudhury, D., Loh, D. H., Dragich, J. M., Hagopian, A. & Colwell, C. S. Select cognitive deficits in vasoactive intestinal peptide deficient mice. BMC Neurosci. 9, 63 (2008).
     PubMed PubMed Central Google Scholar
127. Ueda, H. R. et al. System-level identification of transcriptional circuits underlying mammalian circadian clocks. Nature Genet. 37, 187–192 (2005).
     CAS PubMed Google Scholar
128. Lyons, L. C., Rawashdeh, O. & Eskin, A. Non-ocular circadian oscillators and photoreceptors modulate long term memory formation in Aplysia. J. Biol. Rhythms 21, 245–255 (2006).
     PubMed PubMed Central Google Scholar
129. Tanoue, S., Krishnan, P., Krishnan, B., Dryer, S. E. & Hardin, P. E. Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila. Curr. Biol. 14, 638–649 (2004).
     CAS PubMed Google Scholar
130. Granados-Fuentes, D., Prolo, L. M., Abraham, U. & Herzog, E. D. The suprachiasmatic nucleus entrains, but does not sustain, circadian rhythmicity in the olfactory bulb. J. Neurosci. 24, 615–619 (2004).
     CAS PubMed PubMed Central Google Scholar
131. Granados-Fuentes, D., Tseng, A. & Herzog, E. D. A circadian clock in the olfactory bulb controls olfactory responsivity. J. Neurosci. 26, 12219–12225 (2006).
     CAS PubMed PubMed Central Google Scholar
132. Gerstner, J. R., Vander Heyden, W. M., Lavaute, T. M. & Landry, C. F. Profiles of novel diurnally regulated genes in mouse hypothalamus: expression analysis of the cysteine and histidine-rich domain-containing, zinc-binding protein 1, the fatty acid-binding protein 7 and the GTPase, ras-like family member 11b. Neuroscience 139, 1435–1448 (2006).
     CAS PubMed Google Scholar
133. Wang, L. M. et al. Expression of the circadian clock gene Period2 in the hippocampus: possible implications for synaptic plasticity and learned behaviour. ASN Neuro 1, e00012 (2009).
     PubMed PubMed Central Google Scholar
134. Ma, W. P. et al. Exposure to chronic constant light impairs spatial memory and influences long-term depression in rats. Neurosci. Res. 59, 224–230 (2007).
     PubMed Google Scholar
135. Castro, J. P. et al. Effects of long-term continuous exposure to light on memory and anxiety in mice. Physiol. Behav. 86, 218–223 (2005).
     CAS PubMed Google Scholar
136. Devan, B. D. et al. Circadian phase-shifted rats show normal acquisition but impaired long-term retention of place information in the water task. Neurobiol. Learn. Mem. 75, 51–62 (2001).
     CAS PubMed Google Scholar
137. Craig, L. A. & McDonald, R. J. Chronic disruption of circadian rhythms impairs hippocampal memory in the rat. Brain Res. Bull. 76, 141–151 (2008).
     PubMed Google Scholar
138. Ruby, N. F. et al. Hippocampal-dependent learning requires a functional circadian system. Proc. Natl Acad. Sci. USA 105, 15593–15598 (2008).
     CAS PubMed PubMed Central Google Scholar
139. Reijmers, L. G., Leus, I. E., Burbach, J. P., Spruijt, B. M. & van Ree, J. M. Social memory in the rat: circadian variation and effect of circadian rhythm disruption. Physiol. Behav. 72, 305–309 (2001).
     CAS PubMed Google Scholar
140. Nader, N., Chrousos, G. P. & Kino, T. Interactions of the circadian CLOCK system and the HPA axis. Trends Endocrinol. Metab. 21, 277–286 (2010).
     CAS PubMed PubMed Central Google Scholar
141. McEwen, B. S. Plasticity of the hippocampus: adaptation to chronic stress and allostatic load. Ann. N.Y Acad. Sci. 933, 265–277 (2001).
     CAS PubMed Google Scholar
142. Kim, J. J. & Diamond, D. M. The stressed hippocampus, synaptic plasticity and lost memories. Nature Rev. Neurosci. 3, 453–462 (2002).
     CAS Google Scholar
143. Gerstner, J. R. The aging clock: to 'BMAL'icious toward learning and memory. Aging (Albany, N. Y.) 2, 251–254 (2010).
     CAS Google Scholar
144. Rawashdeh, O. & Stehle, J. H. Ageing or NOT, clock genes are important for memory processes: an interesting hypothesis raising many questions. Aging (Albany N. Y.) 2, 259–260 (2010).
     Google Scholar
145. Roth, T. L. & Sweatt, J. D. Rhythms of memory. Nature Neurosci. 11, 993–994 (2008).
     CAS PubMed Google Scholar
146. Sanada, K., Okano, T. & Fukada, Y. Mitogen-activated protein kinase phosphorylates and negatively regulates basic helix-loop-helix-PAS transcription factor BMAL1. J. Biol. Chem. 277, 267–271 (2002).
     CAS PubMed Google Scholar
147. Obrietan, K., Impey, S. & Storm, D. R. Light and circadian rhythmicity regulate MAP kinase activation in the suprachiasmatic nuclei. Nature Neurosci. 1, 693–700 (1998).
     CAS PubMed Google Scholar
148. Dolmetsch, R. E., Pajvani, U., Fife, K., Spotts, J. M. & Greenberg, M. E. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294, 333–339 (2001).
     CAS PubMed Google Scholar
149. Weber, F., Hung., H. C., Maurer, C. & Kay, S. A. Second messenger and Ras/MAPK signalling pathways regulate CLOCK/CYCLE-dependent transcription. J. Neurochem. 98, 248–257 (2006).
     CAS PubMed Google Scholar
150. Richter, H. G. et al. The circadian timing system: making sense of day/night gene expression. Biol. Res. 37, 11–28 (2004).
     CAS PubMed Google Scholar

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