Aging impairs protein-synthesis-dependent long-term memory in Drosophila

Journal of Neuroscience

Volumn 35, Issue 3, 2015, Pages 1173-1180

  Tonoki, Ayako ^a,b   Davis, Ronald L ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b CHIBA UNIVERSITY   (Japan)

Author keywords

Drosophila; Long term memory

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DYNAMIN; GREEN FLUORESCENT PROTEIN;

AGING; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; FEMALE; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; NERVE CELL NETWORK; NERVE FIBER; NEUROPIL; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; MUSHROOM BODY; NERVE CELL; ODOR; PHYSIOLOGY; SMELLING;

AGING; ANIMALS; DROSOPHILA; MEMORY, LONG-TERM; MUSHROOM BODIES; NERVE NET; NEURONS; ODORS; OLFACTORY PERCEPTION; PROTEIN BIOSYNTHESIS; SMELL;

EID: 84921457618     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0978-14.2015     Document Type: Article

References (29)

1. Akalal DB, Yu D, Davis RL (2010) A late-phase, long-term memory trace forms in the γ neurons of Drosophila mushroom bodies after olfactory classical conditioning. J Neurosci 30:16699-16708. CrossRef Medline
2. Akalal DB, Yu D, Davis RL (2011) The long-term memory trace formed in the Drosophila α/β mushroom body neurons is abolished in long-term memory mutants. J Neurosci 31:5643-5647. CrossRef Medline
3. Beck CD, Schroeder B, Davis RL (2000) Learning performance of normal and mutant Drosophila after repeated conditioning trials with discrete stimuli. J Neurosci 20:2944-2953. Medline
4. Cervantes-Sandoval I, Martin-Peña A, Berry JA, Davis RL (2013) Systemlike consolidation of olfactory memories in Drosophila. J Neurosci 33: 9846-9854. CrossRef Medline
5. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL (1998) Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5:38-51. CrossRef Medline
6. Davis RL (2011) Tracesof Drosophilamemory. Neuron 70:8-19. CrossRefMedline
7. Dubnau J, Grady L, Kitamoto T, Tully T (2001) Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411:476-480. CrossRef Medline
8. Feinberg EH, Vanhoven MK, Bendesky A, Wang G, Fetter RD, Shen K, Bargmann CI (2008) GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57: 353-363. CrossRef Medline
9. Gordon MD, Scott K (2009) Motor control in a Drosophila taste circuit. Neuron 61:373-384. CrossRef Medline
10. Keene AC, Stratmann M, Keller A, Perrat PN, Vosshall LB, Waddell S (2004) Diverse odor-conditioned memories require uniquely timed dorsal paired medial neuron output. Neuron 44:521-533. CrossRef Medline
11. Kitamoto T (2001) Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol 47:81-92. CrossRef Medline
12. Krashes MJ, Keene AC, Leung B, Armstrong JD, Waddell S (2007) Sequential use of mushroom body neuron subsets during Drosophila odor memory processing. Neuron 53:103-115. CrossRef Medline
13. Lee PT, Lin HW, Chang YH, Fu TF, Dubnau J, Hirsh J, Lee T, Chiang AS (2011) Serotonin-mushroom body circuit modulating the formation of anesthesia-resistant memory in Drosophila. Proc Natl Acad Sci U S A 108: 13794-13799. CrossRef Medline
14. Lee T, Lee A, Luo L (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126:4065-4076. Medline
15. McGuire SE, Le PT, Davis RL (2001) The role of Drosophila mushroom body signaling in olfactory memory. Science 293:1330-1333. CrossRef Medline
16. Pagani MR, Oishi K, Gelb BD, Zhong Y (2009) The phosphatase SHP2 regulates the spacing effect for long-term memory induction. Cell 139:186-198. CrossRef Medline
17. Pascual A, Préat T (2001) Localization of long-term memory within the Drosophila mushroom body. Science 294:1115-1117. CrossRef Medline
18. Perazzona B, Isabel G, Preat T, Davis RL (2004) The role of cAMP response element-binding protein in Drosophila long-term memory. J Neurosci 24:8823-8828. CrossRef Medline
19. Pitman JL, Huetteroth W, Burke CJ, Krashes MJ, Lai SL, Lee T, Waddell S (2011) A pair of inhibitory neurons are required to sustain labile memory in the Drosophila mushroom body. Curr Biol 21:855-861. CrossRef Medline
20. Qin H, Cressy M, Li W, Coravos JS, Izzi SA, Dubnau J (2012) Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila. Curr Biol 22:608-614. CrossRef Medline
21. Tamura T, Chiang AS, Ito N, Liu HP, Horiuchi J, Tully T, Saitoe M (2003) Aging specifically impairs amnesiac-dependent memory in Drosophila. Neuron 40:1003-1011. CrossRef Medline
22. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6:875-881. CrossRef Medline
23. Tonoki A, Davis RL (2012) Aging impairs intermediate-term behavioral memory by disrupting the dorsal paired medial neuron memory trace. Proc Natl Acad Sci U S A 109:6319-6324. CrossRef Medline
24. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157:263-277. CrossRef Medline
25. Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79:35-47. CrossRef Medline
26. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG (2000) The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103:805-813. CrossRef Medline
27. Wang Y, Mamiya A, Chiang AS, Zhong Y (2008) Imaging of an early memory trace in the Drosophila mushroom body. J Neurosci 28:4368-4376. CrossRef Medline
28. Yu D, Keene AC, Srivatsan A, Waddell S, Davis RL (2005) Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning. Cell 123:945-957. CrossRef Medline
29. Yu D, Akalal DB, Davis RL (2006) Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52:845-855. CrossRef Medline