Larval population density alters adult sleep in wild-type Drosophila melanogaster but not in Amnesiac mutant flies

Brain Sciences

Volumn 4, Issue 3, 2014, Pages 453-470

  Chi, Michael W ^a   Griffith, Leslie C ^a   Vecsey, Christopher G ^a,b  

^a BRANDEIS UNIVERSITY   (United States)

^b SWARTHMORE COLLEGE   (United States)

Author keywords

Amnesiac; Development; Drosophila; Or83b; Population density; Sleep; Social isolation and enrichment

Indexed keywords

AMNESIAC GENE; ARTICLE; BRAIN DEVELOPMENT; DROSOPHILA MELANOGASTER; EXPERIMENTAL DESIGN; FEMALE; GENE; GENE MUTATION; LARVAL DEVELOPMENT; NONHUMAN; OLFACTORY RECEPTOR; PHYSIOLOGY; POPULATION DENSITY; QUANTITATIVE ANALYSIS; SLEEP PATTERN; SOCIAL ISOLATION;

EID: 84961176026     PISSN: None     EISSN: 20763425     Source Type: Journal    
DOI: 10.3390/brainsci4030453     Document Type: Article

References (67)

1. Banks, S.; Dinges, D.F. Behavioral and physiological consequences of sleep restriction. J. Clin. Sleep Med. 2007, 3, 519-528.
2. Durmer, J.S.; Dinges, D.F. Neurocognitive consequences of sleep deprivation. Semin. Neurol. 2005, 25, 117-129.
3. Mignot, E. Why we sleep: The temporal organization of recovery. PLoS Biol. 2008, 6, e106; doi:10.1371/journal.pbio.0060106.
4. Rechtschaffen, A.; Bergmann, B.M.; Everson, C.A.; Kushida, C.A.; Gilliland, M.A. Sleep deprivation in the rat: X. Integration and discussion of the findings. Sleep 1989, 12, 68-87.
5. Mackiewicz, M.; Naidoo, N.; Zimmerman, J.E.; Pack, A.I. Molecular mechanisms of sleep and wakefulness. Ann. N. Y. Acad. Sci. 2008, 1129, 335-349.
6. Murillo-Rodriguez, E.; Arias-Carrion, O.; Zavala-Garcia, A.; Sarro-Ramirez, A.; Huitron-Resendiz, S.; Arankowsky-Sandoval, G. Basic sleep mechanisms: An integrative review. Cent. Nerv. Syst. Agents Med. Chem. 2012, 12, 38-54.
7. Potdar, S.; Sheeba, V. Lessons from sleeping flies: Insights from Drosophila melanogaster on the neuronal circuitry and importance of sleep. J. Neurogenet. 2013, 27, 23-42.
8. Huber, R.; Hill, S.L.; Holladay, C.; Biesiadecki, M.; Tononi, G.; Cirelli, C. Sleep homeostasis in Drosophila melanogaster. Sleep 2004, 27, 628-639.
9. Borbely, A.A.; Achermann, P. Sleep homeostasis and models of sleep regulation. J. Biol. Rhythms 1999, 14, 557-568.
10. Shaw, P.J.; Cirelli, C.; Greenspan, R.J.; Tononi, G. Correlates of sleep and waking in Drosophila melanogaster. Science 2000, 287, 1834-1837.
11. Borbely, A.A.; Baumann, F.; Brandeis, D.; Strauch, I.; Lehmann, D. Sleep deprivation: Effect on sleep stages and EEG power density in man. Electroencephalogr. Clin. Neurophysiol. 1981, 51, 483-495.
12. Venken, K.J.; Simpson, J.H.; Bellen, H.J. Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 2011, 72, 202-230.
13. Adams, M.D.; Celniker, S.E.; Holt, R.A.; Evans, C.A.; Gocayne, J.D.; Amanatides, P.G.; Scherer, S.E.; Li, P.W.; Hoskins, R.A.; Galle, R.F., et al. The genome sequence of Drosophila melanogaster. Science 2000, 287, 2185-2195.
14. Sokolowski, M.B. Drosophila: Genetics meets behavior. Nat. Rev. Genet. 2001, 2, 879-890.
15. Cirelli, C.; Bushey, D. Sleep and wakefulness in Drosophila melanogaster. Ann. N. Y. Acad. Sci. 2008, 1129, 323-329.
16. Hendricks, J.C.; Sehgal, A.; Pack, A.I. The need for a simple animal model to understand sleep. Prog. Neurobiol. 2000, 61, 339-351.
17. Hendricks, J.C.; Finn, S.M.; Panckeri, K.A.; Chavkin, J.; Williams, J.A.; Sehgal, A.; Pack, A.I. Rest in Drosophila is a sleep-like state. Neuron 2000, 25, 129-138.
18. Nitz, D.A.; van Swinderen, B.; Tononi, G.; Greenspan, R.J. Electrophysiological correlates of rest and activity in Drosophila melanogaster. Curr. Biol. 2002, 12, 1934-1940.
19. Van Alphen, B.; Yap, M.H.; Kirszenblat, L.; Kottler, B.; van Swinderen, B. A dynamic deep sleep stage in Drosophila. J. Neurosci. 2013, 33, 6917-6927.
20. Zimmerman, J.E.; Naidoo, N.; Raizen, D.M.; Pack, A.I. Conservation of sleep: Insights from non-mammalian model systems. Trends Neurosci. 2008, 31, 371-376.
21. Ganguly-Fitzgerald, I.; Donlea, J.; Shaw, P.J. Waking experience affects sleep need in Drosophila. Science 2006, 313, 1775-1781.
22. Donlea, J.M.; Ramanan, N.; Shaw, P.J. Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 2009, 324, 105-108.
23. Andretic, R.; Shaw, P.J. Essentials of sleep recordings in Drosophila: Moving beyond sleep time. Methods Enzymol. 2005, 393, 759-772.
24. Donelson, N.; Kim, E.Z.; Slawson, J.B.; Vecsey, C.G.; Huber, R.; Griffith, L.C. High-resolution positional tracking for long-term analysis of Drosophila sleep and locomotion using the -tracker{norm of matrix} program. PLos One 2012, 7, e37250; doi:10.1371/journal.pone.0037250.
25. Gilestro, G.F. Video tracking and analysis of sleep in Drosophila melanogaster. Nat. Protoc. 2012, 7, 995-1007.
26. Hitier, R.; Heisenberg, M.; Preat, T. Abnormal mushroom body plasticity in the Drosophila memory mutant amnesiac. Neuroreport 1998, 9, 2717-2719.
27. Stewart, B.A.; McLean, J.R. Population density regulates Drosophila synaptic morphology in a Fasciclin-II-dependent manner. J. Neurobiol. 2004, 61, 392-399.
28. Technau, G.M. Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J. Neurogenet. 1984, 1, 113-126.
29. Heisenberg, M. What do the mushroom bodies do for the insect brain? An introduction. Learn Mem. 1998, 5, 1-10.
30. Zars, T. Behavioral functions of the insect mushroom bodies. Curr. Opin. Neurobiol. 2000, 10, 790-795.
31. Campbell, R.A.; Turner, G.C. The mushroom body. Curr. Biol. 2010, 20, R11-R12.
32. Guo, F.; Yi, W.; Zhou, M.; Guo, A. Go signaling in mushroom bodies regulates sleep in Drosophila. Sleep 2011, 34, 273-281.
33. Joiner, W.J.; Crocker, A.; White, B.H.; Sehgal, A. Sleep in Drosophila is regulated by adult mushroom bodies. Nature 2006, 441, 757-760.
34. Pitman, J.L.; McGill, J.J.; Keegan, K.P.; Allada, R. A dynamic role for the mushroom bodies in promoting sleep in Drosophila. Nature 2006, 441, 753-756.
35. Quinn, W.G.; Sziber, P.P.; Booker, R. The Drosophila memory mutant amnesiac. Nature 1979, 277, 212-214.
36. Waddell, S.; Armstrong, J.D.; Kitamoto, T.; Kaiser, K.; Quinn, W.G. The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 2000, 103, 805-813.
37. Liu, W.; Guo, F.; Lu, B.; Guo, A. Amnesiac regulates sleep onset and maintenance in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 2008, 372, 798-803.
38. Levine, J.D.; Funes, P.; Dowse, H.B.; Hall, J.C. Resetting the circadian clock by social experience in Drosophila melanogaster. Science 2002, 298, 2010-2012.
39. Lone, S.R.; Sharma, V.K. Social synchronization of circadian locomotor activity rhythm in the fruit fly Drosophila melanogaster. J. Exp. Biol. 2011, 214, 3742-3750.
40. Larsson, M.C.; Domingos, A.I.; Jones, W.D.; Chiappe, M.E.; Amrein, H.; Vosshall, L.B. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 2004, 43, 703-714.
41. Yu, D.; Keene, A.C.; Srivatsan, A.; Waddell, S.; Davis, R.L. Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell 2005, 123, 945-957.
42. Balling, A.; Technau, G.M.; Heisenberg, M. Are the structural changes in adult Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants. J. Neurogenet. 1987, 4, 65-73.
43. Folkers, E.; Drain, P.; Quinn, W.G. Radish, a Drosophila mutant deficient in consolidated memory. Proc. Natl. Acad. Sci. USA 1993, 90, 8123-8127.
44. Folkers, E.; Waddell, S.; Quinn, W.G. The Drosophila radish gene encodes a protein required for anesthesia-resistant memory. Proc. Natl. Acad. Sci. USA 2006, 103, 17496-17500.
45. Shioda, S. Pituitary adenylate cyclase-activating polypeptide (PACAP) and its receptors in the brain. Kaibogaku Zasshi 2000, 75, 487-507.
46. Makinodan, M.; Rosen, K.M.; Ito, S.; Corfas, G. A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 2012, 337, 1357-1360.
47. Martin, L.J.; Spicer, D.M.; Lewis, M.H.; Gluck, J.P.; Cork, L.C. Social deprivation of infant rhesus monkeys alters the chemoarchitecture of the brain: I. Subcortical regions. J. Neurosci. 1991, 11, 3344-3358.
48. Miyazaki, T.; Takase, K.; Nakajima, W.; Tada, H.; Ohya, D.; Sano, A.; Goto, T.; Hirase, H.; Malinow, R.; Takahashi, T. Disrupted cortical function underlies behavior dysfunction due to social isolation. J. Clin. Invest. 2012, 122, 2690-2701.
49. Miyazaki, T.; Kunii, M.; Jitsuki, S.; Sano, A.; Kuroiwa, Y.; Takahashi, T. Social isolation perturbs experience-driven synaptic glutamate receptor subunit 4 delivery in the developing rat barrel cortex. Eur. J. Neurosci. 2013, 37, 1602-1609.
50. Siegel, S.J.; Ginsberg, S.D.; Hof, P.R.; Foote, S.L.; Young, W.G.; Kraemer, G.W.; McKinney, W.T.; Morrison, J.H. Effects of social deprivation in prepubescent rhesus monkeys: Immunohistochemical analysis of the neurofilament protein triplet in the hippocampal formation. Brain Res. 1993, 619, 299-305.
51. Struble, R.G.; Riesen, A.H. Changes in cortical dendritic branching subsequent to partial social isolation in stumptailed monkeys. Dev. Psychobiol. 1978, 11, 479-486.
52. Danese, A.; Moffitt, T.E.; Harrington, H.; Milne, B.J.; Polanczyk, G.; Pariante, C.M.; Poulton, R.; Caspi, A. Adverse childhood experiences and adult risk factors for age-related disease: Depression, inflammation, and clustering of metabolic risk markers. Arch. Pediatr. Adolesc. Med. 2009, 163, 1135-1143.
53. Caspi, A.; Harrington, H.; Moffitt, T.E.; Milne, B.J.; Poulton, R. Socially isolated children 20 years later: Risk of cardiovascular disease. Arch. Pediatr. Adolesc. Med. 2006, 160, 805-811.
54. Cacioppo, J.T.; Hawkley, L.C. Social isolation and health, with an emphasis on underlying mechanisms. Perspect. Biol. Med. 2003, 46, S39-S52.
55. Sullivan, R.; Wilson, D.A.; Feldon, J.; Yee, B.K.; Meyer, U.; Richter-Levin, G.; Avi, A.; Michael, T.; Gruss, M.; Bock, J., et al. The International Society for Developmental Psychobiology annual meeting symposium: Impact of early life experiences on brain and behavioral development. Dev. Psychobiol. 2006, 48, 583-602.
56. Koskenvuo, K.; Hublin, C.; Partinen, M.; Paunio, T.; Koskenvuo, M. Childhood adversities and quality of sleep in adulthood: A population-based study of 26,000 Finns. Sleep Med. 2010, 11, 17-22.
57. Greenfield, E.A.; Lee, C.; Friedman, E.L.; Springer, K.W. Childhood abuse as a risk factor for sleep problems in adulthood: Evidence from a U.S. national study. Ann. Behav. Med. 2011, 42, 245-256.
58. Ahmad, S.T.; Steinmetz, S.B.; Bussey, H.M.; Possidente, B.; Seggio, J.A. Larval ethanol exposure alters free-running circadian rhythm and per Locus transcription in adult D. melanogaster period mutants. Behav. Brain Res. 2013, 241, 50-55.
59. Seggio, J.A.; Possidente, B.; Ahmad, S.T. Larval ethanol exposure alters adult circadian free-running locomotor activity rhythm in Drosophila melanogaster. Chronobiol. Int. 2012, 29, 75-81.
60. Helfrich-Forster, C. Differential control of morning and evening components in the activity rhythm of Drosophila melanogaster-Sex-specific differences suggest a different quality of activity. J. Biol. Rhythms 2000, 15, 135-154.
61. Schneider, J.; Dickinson, M.H.; Levine, J.D. Social structures depend on innate determinants and chemosensory processing in Drosophila. Proc. Natl. Acad. Sci. USA 2012, 109, 17174-17179.
62. Schneider, J.; Atallah, J.; Levine, J.D. One, two, and many-A perspective on what groups of Drosophila melanogaster can tell us about social dynamics. Adv. Genet. 2012, 77, 59-78.
63. Lone, S.R.; Sharma, V.K. Or47b receptor neurons mediate sociosexual interactions in the fruit fly Drosophila melanogaster. J. Biol. Rhythms 2012, 27, 107-116.
64. Kent, C.; Azanchi, R.; Smith, B.; Formosa, A.; Levine, J.D. Social context influences chemical communication in D. melanogaster males. Curr. Biol. 2008, 18, 1384-1389.
65. Moore, M.S.; DeZazzo, J.; Luk, A.Y.; Tully, T.; Singh, C.M.; Heberlein, U. Ethanol intoxication in Drosophila: Genetic and pharmacological evidence for regulation by the cAMP signaling pathway. Cell 1998, 93, 997-1007.
66. Tran, S.L.; Welte, M.A. In-vivo centrifugation of Drosophila embryos. J. Vis. Exp. 2010, 40, 2005; doi:10.3791/2005.
67. Levine, J.D.; Funes, P.; Dowse, H.B.; Hall, J.C. Signal analysis of behavioral and molecular cycles. BMC Neurosci. 2002, 3, 1; doi:10.1186/1471-2202-3-1.