title: Shocking revelations and saccharin sweetness in the study of Drosophila olfactory memory.
abstract: It is now almost forty years since the first description of learning in the fruit fly Drosophila melanogaster. Various incarnations of the classic mutagenesis approach envisaged in the early days have provided around one hundred learning defective mutant fly strains. Recent technological advances permit temporal control of neural function in the behaving fly. These approaches have radically changed experiments in the field and have provided a neural circuit perspective of memory formation, consolidation and retrieval. Combining neural perturbations with more classical mutant intervention allows investigators to interrogate the molecular and cellular processes of memory within the defined neural circuits. Here, we summarize some of the progress made in the last ten years that indicates a remarkable conservation of the neural mechanisms of memory formation between flies and mammals. We emphasize that considering an ethologically-relevant viewpoint might provide additional experimental power in studies of Drosophila memory.
authors.affiliation: Centre for Neural Circuits and Behaviour, The University of Oxford, Tinsley Building, Mansfield Road, Oxford, OX1 3SR, United Kingdom.
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Perisse
authors.forename: Christopher
authors.initials: C
authors.lastname: Burke
authors.forename: Wolf
authors.initials: W
authors.lastname: Huetteroth
authors.forename: Scott
authors.initials: S
authors.lastname: Waddell
mesh_terms: D000818:Animals; D001522:Behavior, Animal; D004331:Drosophila melanogaster / Q000502:physiology*; D008568:Memory; D012903:Smell / Q000502:physiology*
references.citation: Science. 2004 Jan 16;303(5656):366-70
references.pmid: 14684826
references.citation: Curr Biol. 2012 Jul 10;22(13):1247-52
references.pmid: 22658595
references.citation: Nature. 1976 Aug 12;262(5569):576-7
references.pmid: 822344
references.citation: Neuron. 2004 Oct 28;44(3):521-33
references.pmid: 15504331
references.citation: Cell Rep. 2012 Oct 25;2(4):991-1001
references.pmid: 23063364
references.citation: J Neurobiol. 2001 May;47(2):81-92
references.pmid: 11291099
references.citation: Nature. 2010 Dec 2;468(7324):686-90
references.pmid: 21124455
references.citation: Neuropharmacology. 2013 Nov;74:18-22
references.pmid: 23439383
references.citation: J Neurosci. 2003 Nov 19;23(33):10495-502
references.pmid: 14627633
references.citation: Cell. 2009 Oct 16;139(2):405-15
references.pmid: 19837039
references.citation: Nat Neurosci. 2006 May;9(5):703-9
references.pmid: 16582903
references.citation: Curr Biol. 2011 May 24;21(10):855-61
references.pmid: 21530258
references.citation: Curr Biol. 2011 May 24;21(10):848-54
references.pmid: 21530256
references.citation: J Cell Biol. 2010 Feb 22;188(4):565-79
references.pmid: 20176924
references.citation: Curr Biol. 2009 Aug 25;19(16):1341-50
references.pmid: 19646879
references.citation: Curr Biol. 2010 Dec 21;20(24):2234-40
references.pmid: 21129969
references.citation: Neuron. 2009 Feb 12;61(3):373-84
references.pmid: 19217375
references.citation: Nat Neurosci. 2011 Jun 19;14(7):903-10
references.pmid: 21685917
references.citation: Nature. 2012 Dec 20;492(7429):433-7
references.pmid: 23103875
references.citation: Nature. 2007 Jul 12;448(7150):151-6
references.pmid: 17625558
references.citation: Genome Res. 2005 Mar;15(3):376-84
references.pmid: 15710747
references.citation: Nat Neurosci. 2009 Jan;12(1):53-9
references.pmid: 19043409
references.citation: Neuron. 2007 Jan 4;53(1):103-15
references.pmid: 17196534
references.citation: Nature. 1998 Jul 9;394(6689):192-5
references.pmid: 9671304
references.citation: Neuron. 2006 Mar 16;49(6):833-44
references.pmid: 16543132
references.citation: Nature. 2008 Apr 24;452(7190):956-60
references.pmid: 18344978
references.citation: J Neurosci. 2007 Jul 18;27(29):7640-7
references.pmid: 17634358
references.citation: Science. 2011 May 6;332(6030):721-5
references.pmid: 21551062
references.citation: Curr Biol. 2010 Aug 24;20(16):1445-51
references.pmid: 20637624
references.citation: Curr Biol. 2006 Aug 8;16(15):1524-30
references.pmid: 16890528
references.citation: J Comp Physiol Psychol. 1973 Jan;82(1):137-43
references.pmid: 4684968
references.citation: J Neurogenet. 2000 Jan;13(4):233-55
references.pmid: 10858822
references.citation: Cell. 1994 Oct 7;79(1):35-47
references.pmid: 7923375
references.citation: Cell. 2005 Dec 2;123(5):945-57
references.pmid: 16325586
references.citation: Curr Biol. 2006 Sep 5;16(17):1741-7
references.pmid: 16950113
references.citation: Adv Exp Med Biol. 2008;628:102-14
references.pmid: 18683641
references.citation: Cell. 2009 Oct 16;139(2):416-27
references.pmid: 19837040
references.citation: Int Rev Neurobiol. 2011;99:139-67
references.pmid: 21906539
references.citation: J Neurosci. 2012 Jun 13;32(24):8138-48
references.pmid: 22699895
references.citation: Neuron. 2002 Aug 29;35(5):951-60
references.pmid: 12372288
references.citation: Cell. 2010 Feb 19;140(4):579-89
references.pmid: 20178749
references.citation: Nature. 2008 Mar 27;452(7186):473-7
references.pmid: 18305480
references.citation: Proc Natl Acad Sci U S A. 1986 Dec;83(24):9313-7
references.pmid: 3025834
references.citation: Neuron. 2012 May 10;74(3):530-42
references.pmid: 22578504
references.citation: J Comp Physiol A. 1985 Sep;157(2):263-77
references.pmid: 3939242
references.citation: Nat Neurosci. 2005 Sep;8(9):1263-8
references.pmid: 16116447
references.citation: J Neurosci. 2011 Aug 17;31(33):11772-85
references.pmid: 21849538
references.citation: Genes Brain Behav. 2009 Jun;8(4):407-15
references.pmid: 19220480
references.citation: Neuron. 2008 Jul 31;59(2):311-21
references.pmid: 18667158
references.citation: Science. 2001 Aug 17;293(5533):1330-3
references.pmid: 11397912
references.citation: Cell. 2010 Apr 30;141(3):536-48
references.pmid: 20434990
references.citation: Proc Natl Acad Sci U S A. 2013 May 7;110(19):7898-903
references.pmid: 23610406
references.citation: J Neurosci. 2012 Oct 3;32(40):13819-40
references.pmid: 23035093
references.citation: Curr Biol. 2011 May 10;21(9):751-5
references.pmid: 21514154
references.citation: J Neurogenet. 2011 Mar;25(1-2):1-6
references.pmid: 21510718
references.citation: Nature. 2008 Jul 10;454(7201):217-20
references.pmid: 18548007
references.citation: Neuron. 2008 Sep 25;59(6):1009-23
references.pmid: 18817738
references.citation: Cell. 2004 Jun 25;117(7):965-79
references.pmid: 15210116
references.citation: Neuron. 2010 Sep 23;67(6):1034-47
references.pmid: 20869599
references.citation: Proc Natl Acad Sci U S A. 2009 Aug 4;106(31):13070-5
references.pmid: 19625621
references.citation: Curr Opin Neurobiol. 2004 Dec;14(6):737-44
references.pmid: 15582377
references.citation: Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9715-20
references.pmid: 18621688
references.citation: Nat Biotechnol. 2001 Feb;19(2):137-41
references.pmid: 11175727
references.citation: J Neurosci. 2010 Dec 8;30(49):16699-708
references.pmid: 21148009
references.citation: J Comp Neurol. 2008 Jun 10;508(5):711-55
references.pmid: 18395827
references.citation: Cell. 1994 Oct 7;79(1):49-58
references.pmid: 7923376
references.citation: Cell. 2007 Mar 23;128(6):1187-203
references.pmid: 17382886
references.citation: J Neurosci. 2005 Oct 5;25(40):9069-79
references.pmid: 16207866
references.citation: Cell. 2007 Feb 9;128(3):601-12
references.pmid: 17289577
references.citation: Curr Biol. 2012 Nov 6;22(21):1981-9
references.pmid: 23063437
references.citation: Cell. 2009 Oct 2;139(1):186-98
references.pmid: 19804763
references.citation: Cell. 2005 Apr 8;121(1):141-52
references.pmid: 15820685
references.citation: Neuron. 2006 Dec 7;52(5):845-55
references.pmid: 17145505
references.citation: Curr Biol. 2008 Nov 11;18(21):1668-74
references.pmid: 18951022
references.citation: J Neurosci. 2011 Jun 29;31(26):9696-707
references.pmid: 21715635
references.citation: Curr Biol. 2011 May 10;21(9):746-50
references.pmid: 21514159
references.citation: Proc Natl Acad Sci U S A. 2011 Aug 16;108(33):13794-9
references.pmid: 21808003
references.citation: Proc Natl Acad Sci U S A. 1983 Mar;80(5):1482-6
references.pmid: 6572401
references.citation: Science. 1995 May 12;268(5212):869-73
references.pmid: 7754370
references.citation: Nat Neurosci. 2013 May;16(5):526-8
references.pmid: 23542692
references.citation: Science. 2003 Dec 5;302(5651):1765-8
references.pmid: 14657498
references.citation: Science. 2013 Jan 25;339(6118):440-2
references.pmid: 23349289
references.citation: Cell. 2012 Nov 21;151(5):1113-25
references.pmid: 23178127
references.citation: Neuron. 2007 Apr 5;54(1):89-103
references.pmid: 17408580
references.citation: J Neurogenet. 2012 Jun;26(2):238-44
references.pmid: 22436011
references.citation: Nat Rev Neurosci. 2007 May;8(5):341-54
references.pmid: 17453015
references.citation: Science. 2001 Nov 2;294(5544):1030-8
references.pmid: 11691980
references.citation: Science. 2012 Feb 10;335(6069):678-85
references.pmid: 22323813
references.citation: Science. 2004 May 14;304(5673):1024-7
references.pmid: 15143285
references.citation: J Comp Neurol. 2009 Dec 20;517(6):808-24
references.pmid: 19844895
references.citation: Proc Natl Acad Sci U S A. 2006 Nov 14;103(46):17496-500
references.pmid: 17088531
references.citation: Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8123-7
references.pmid: 8367473
references.citation: Neuron. 2001 May;30(2):537-52
references.pmid: 11395013
references.citation: Neuron. 2003 Dec 4;40(5):1003-11
references.pmid: 14659098
references.citation: J Neurosci. 2008 Mar 19;28(12):3103-13
references.pmid: 18354013
references.citation: Proc Natl Acad Sci U S A. 2010 Nov 23;107(47):20553-8
references.pmid: 21059961
references.citation: Development. 1993 Jun;118(2):401-15
references.pmid: 8223268
references.citation: Neuron. 2008 Feb 7;57(3):353-63
references.pmid: 18255029
references.citation: Nat Neurosci. 2007 Nov;10(11):1474-82
references.pmid: 17922008
references.citation: Nature. 2013 May 2;497(7447):113-7
references.pmid: 23615618
references.citation: Biochem Biophys Res Commun. 2013 Jun 21;436(1):35-40
references.pmid: 23707718
references.citation: Neuron. 2013 Sep 4;79(5):945-56
references.pmid: 24012007
references.citation: Nature. 2012 Dec 6;492(7427):66-71
references.pmid: 23172146
references.citation: Curr Biol. 2012 Apr 10;22(7):608-14
references.pmid: 22425153
references.citation: Nat Rev Neurosci. 2003 Apr;4(4):266-75
references.pmid: 12671643
references.citation: J Neurosci. 2009 Feb 4;29(5):1573-9
references.pmid: 19193904
references.citation: Nature. 1981 Jan 1;289(5793):79-81
references.pmid: 6256649
references.citation: Learn Mem. 2006 Sep-Oct;13(5):659-68
references.pmid: 16980542
references.citation: Behav Neurosci. 2011 Dec;125(6):797-824
references.pmid: 22122145
references.citation: Neuron. 1991 Jan;6(1):71-82
references.pmid: 1702651
references.citation: Nat Methods. 2011 Mar;8(3):253-9
references.pmid: 21297621
references.citation: Nat Methods. 2011 Mar;8(3):260-6
references.pmid: 21297619
references.citation: Curr Opin Neurobiol. 2013 Jun;23(3):324-9
references.pmid: 23391527
references.citation: J Exp Biol. 2003 Mar;206(Pt 5):843-55
references.pmid: 12547939
references.citation: J Neurosci. 2004 Jul 21;24(29):6507-14
references.pmid: 15269261
references.citation: Science. 2000 Apr 28;288(5466):672-5
references.pmid: 10784450
references.citation: Proc Natl Acad Sci U S A. 1976 May;73(5):1684-8
references.pmid: 818641
references.citation: Eur J Neurosci. 2011 Jan;33(1):143-52
references.pmid: 21070389
references.citation: Science. 2013 Jan 25;339(6118):443-6
references.pmid: 23349290
references.citation: Cell. 1992 Feb 7;68(3):479-89
references.pmid: 1739965
references.citation: Cell. 2000 Nov 22;103(5):805-13
references.pmid: 11114336
references.citation: Curr Biol. 2009 Oct 13;19(19):1654-9
references.pmid: 19781943
references.citation: J Neurosci. 2004 Jun 30;24(26):6037-47
references.pmid: 15229251
references.citation: Science. 2013 Apr 5;340(6128):91-5
references.pmid: 23559253
references.citation: Nat Methods. 2011 Mar;8(3):231-7
references.pmid: 21473015
references.citation: Network. 2000 May;11(2):119-29
references.pmid: 10880002
references.citation: PLoS Genet. 2012;8(7):e1002768
references.pmid: 22807684
references.citation: Front Behav Neurosci. 2010 Dec 31;4:192
references.pmid: 21258642
references.citation: Nature. 2012 Aug 23;488(7412):512-6
references.pmid: 22810589
references.citation: Curr Biol. 2011 Oct 11;21(19):1647-53
references.pmid: 21962716
references.citation: Proc Natl Acad Sci U S A. 1974 Mar;71(3):708-12
references.pmid: 4207071
references.citation: Nat Neurosci. 2012 Feb 26;15(4):592-9
references.pmid: 22366756
references.citation: Proc Natl Acad Sci U S A. 2001 Dec 18;98(26):15336-41
references.pmid: 11742061
references.citation: Neuron. 2004 Sep 2;43(5):663-72
references.pmid: 15339648
references.citation: Cell. 2002 Apr 19;109(2):229-41
references.pmid: 12007409
references.citation: Fly (Austin). 2009 Jan-Mar;3(1):3-9
references.pmid: 19164943
references.citation: Cell. 1984 May;37(1):205-15
references.pmid: 6327051
references.citation: J Neurophysiol. 2008 Feb;99(2):734-46
references.pmid: 18094099
references.citation: J Neurosci. 2009 Mar 18;29(11):3343-53
references.pmid: 19295141