Gustatory learning and processing in the Drosophila mushroom bodies

Journal of Neuroscience

Volumn 35, Issue 15, 2015, Pages 5950-5958

  Kirkhart, Colleen ^a   Scott, Kristin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Drosophila; Gustatory; Learning; Memory; Taste aversion

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BEHAVIOR; BRAIN REGION; CONDITIONED REFLEX; CONDITIONING; DENDRITE; DOPAMINERGIC NERVE CELL; FEMALE; GENETIC ANALYSIS; GUSTATORY SYSTEM; IMAGING; LEARNING; LEARNING AND MEMORY TEST; MUSHROOM BODY; NONHUMAN; PRIORITY JOURNAL; SENSORY STIMULATION; SHORT TERM MEMORY; SIGNAL TRANSDUCTION; STATE DEPENDENT LEARNING; SYNAPTIC INHIBITION; TASTE; TASTE AVERSION; ANIMAL; DROSOPHILA; GENETICS; HEMISPHERIC DOMINANCE; METABOLISM; OLFACTORY RECEPTOR; PHYSIOLOGY; SENSORY NERVE; SENSORY NERVE CELL; TRANSGENIC ANIMAL;

CALCIUM; DROSOPHILA PROTEIN; NERVE PROTEIN; OLFACTORY RECEPTOR; OR83B PROTEIN, DROSOPHILA; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPA1 PROTEIN, DROSOPHILA; TYROSINE 3 MONOOXYGENASE;

AFFERENT PATHWAYS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CALCIUM; CONDITIONING, CLASSICAL; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; FUNCTIONAL LATERALITY; MEMORY, SHORT-TERM; MUSHROOM BODIES; NERVE TISSUE PROTEINS; RECEPTORS, ODORANT; SENSORY RECEPTOR CELLS; TASTE; TRPC CATION CHANNELS; TYROSINE 3-MONOOXYGENASE;

EID: 84929240851     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3930-14.2015     Document Type: Article

References (48)

1. Akerboom J, Chen TW, War dill TJ, Tian L, Marvin JS, Mutlu S, Calderón NC, Esposti F, Borghuis BG, Sun XR, Gordus A, Orger MB, Portugues R, Engert F, Macklin JJ, Filosa A, Aggarwal A, Kerr RA, Takagi R, Kracun S, Shigetomi E, Khakh BS, Baier H, Lagnado L, Wang SS, Bargmann CI, Kimmel BE, Jayaraman V, Svoboda K, Kim DS, Schreiter ER, Looger LL (2011) Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32:13819-13840. CrossRef Medline
2. Aso Y, Grübel K, Busch S, Friedrich AB, Siwanowicz I, Tanimoto H (2009) The mushroom body of adult Drosophila characterized by GAL4 drivers. J Neurogenet 23:156-172. CrossRef Medline
3. Blum AL, Li W, Cressy M, Dubnau J (2009) Short-and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Curr Biol 19:1341-1350. CrossRef Medline
4. Burke CJ, Huetteroth W, Owald D, Perisse E, Krashes MJ, Das G, GohI D, Silies M, Certel S, Waddell S (2012) Layered reward signalling through octopamine and dopamine in Drosophila. Nature 492:433-437. CrossRef Medline
5. Caron SJ, Ruta V, Abbott LF, Axel R (2013) Random convergence of olfactory inputs in the Drosophila mushroom body. Nature 497:113-117. CrossRef Medline
6. Cassenaer S, Laurent G (2012) Conditional modulation of spike-timing-dependent plasticity for olfactory learning. Nature 482:47-52. CrossRef Medline
7. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS (2012) Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295-300. CrossRef Medline
8. Claridge-Chang A, Roorda RD, Vrontou E, Sjulson L, Li H, Hirsh J, Miesen-böck G (2009) Writing memories with light-addressable reinforcement circuitry. Cell 139:405-415. CrossRef Medline
9. Cole SH, Carney GE, McClung CA, Willard SS, Taylor BJ, Hirsh J (2005) Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: distinct roles for neural tyramine and octopamine in female fertility. J Biol Chem 280:14948-14955. CrossRef Medline
10. Connolly JB, Roberts IJ, Armstrong JD, Kaiser K, Forte M, TullyT, O’Kane CJ (1996) Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274:2104-2107. CrossRef Medline
11. Das G, Klappenbach M, Vrontou E, Perisse E, Clark CM, Burke CJ, Waddell S (2014) Drosophila learn opposing components of a compound food stimulus. Curr Biol 24:1723-1730. CrossRef Medline
12. Davis RL (2005) Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu Rev Neurosci 28:275-302. CrossRef Medline
13. Farris SM (2008) Tritocerebral tract input to the insect mushroom bodies. Arthropod Struct Dev 37:492-503. CrossRef Medline
14. Friggi-Grelin F, Coulom H, Meller M, Gomez D, Hirsh J, Birman S (2003) Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J Neurobiol 54:618-627. CrossRef Medline
15. Gruntman E, Turner GC (2013) Integration of the olfactory code across dendritic claws of single mushroom body neurons. Nat Neurosci 16: 1821-1829. CrossRef Medline
16. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454:217-220. CrossRef Medline
17. Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266-275. CrossRef Medline
18. Leiss F, Groh C, Butcher NJ, Meinertzhagen IA, Tavosanis G (2009) Synaptic organization in the adult Drosophila mushroom body calyx. J Comp Neurol 517:808-824. CrossRef Medline
19. Keene AC, Masek P (2012) Optogenetic induction of aversive taste memory. Neuroscience 222:173-180. CrossRef Medline
20. Keene AC, Waddell S (2007) Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 8:341-354. CrossRef Medline
21. Keleman K, Krüttner S, Alenius M, Dickson BJ (2007) Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat Neurosci 10:1587-1593. CrossRef Medline
22. 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
23. 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
24. Lai SL, Lee T (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9:703-709. CrossRef Medline
25. Liman ER, Zhang YV, Montell C (2014) Peripheral coding of taste. Neuron 81:984-1000. CrossRef Medline
26. Liu C, Plaçais PY, Yamagata N, Pfeiffer BD, Aso Y, Friedrich AB, Siwanowicz G, Rubin GM, Preat T, Tanimoto H (2012) A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488:512-516. CrossRef Medline
27. Mann K, Gordon MD, Scott K (2013) A pair of interneurons influences the choice between feeding and locomotion in Drosophila. Neuron 79:754-765. CrossRef Medline
28. Mao Z, Davis RL (2009) Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front Neural Circuits 3:5. CrossRef Medline
29. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, Scott K (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49:285-295. CrossRef Medline
30. Martini SR, Davis RL (2005) The dachshund gene is required for the proper guidance and branching of mushroom body axons in Drosophila melano-gaster. J Neurobiol 64:133-144. CrossRef Medline
31. Masek P, Scott K (2010) Limited taste discrimination in Drosophila. Proc Natl Acad Sci U S A 107:14833-14838. CrossRef Medline
32. McGuire SE, Le PT, Davis RL (2001) The role of Drosophila mushroom body signaling in olfactory memory. Science 293:1330-1333. CrossRef Medline
33. Menzel R (2014) The insect mushroom body, an experience-dependent recoding device. J Physiol Paris 108:84-95. CrossRef Medline
34. Murthy M, Fiete I, Laurent G (2008) Testing odor response stereotypy in the Drosophila mushroom body. Neuron 59:1009-1023. CrossRef Medline
35. O’Dell KM, Armstrong JD, Yang MY, Kaiser K (1995) Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 15:55-61. CrossRef Medline
36. Schulz RA, Chromey C, Lu MF, Zhao B, Olson EN (1996) Expression of the D-MEF2 transcription in the Drosophila brain suggests a role in neuronal cell differentiation. Oncogene 12:1827-1831. Medline
37. Sitaraman D, Zars M, Laferriere H, Chen YC, Sable-Smith A, Kitamoto T, Rottinghaus GE, Zars T (2008) Serotonin is necessary for place memory in Drosophila. Proc Natl Acad Sci USA 105:5579-5584. CrossRef Medline
38. Sitaraman D, LaFerriere H, Birman S, Zars T (2012) Serotonin is critical for rewarded olfactory short-term memory in Drosophila. J Neurogenet 26: 238-244. CrossRef Medline
39. Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3-26. CrossRef Medline
40. Tanaka NK, Tanimoto H, Ito K (2008) Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711-755. CrossRef Medline
41. Tomchik SM (2013) Dopaminergic neurons encode a distributed, asymmetric representation of temperature in Drosophila. J Neurosci 33:2166-2176. CrossRef Medline
42. Trannoy S, Redt-Clouet C, Dura JM, Preat T (2011) Parallel processing of appetitive short-and long-term memories in Drosophila. Curr Biol 21: 1647-1653. CrossRef Medline
43. Turner GC, Bazhenov M, Laurent G (2008) Olfactory representations by Drosophila mushroom body neurons. J Neurophysiol 99:734-746. CrossRef Medline
44. van Swinderen B (2009) Fly memory: a mushroom body story in parts. Curr Biol 19:R855-R857. CrossRef Medline
45. Wang Z, Singhvi A, Kong P, Scott K (2004) Taste representations in the Drosophila brain. Cell 117:981-991. CrossRef Medline
46. Yang MY, Armstrong JD, Vilinsky I, Strausfeld NJ, Kaiser K (1995) Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15:45-54. CrossRef Medline
47. Zars T (2000) Behavioral functions of the insect mushroom bodies. Curr Opin Neurobiol 10:790-795. CrossRef Medline
48. Zars T, Fischer M, Schulz R, Heisenberg M (2000) Localization of a shortterm memory in Drosophila. Science 288:672-675. CrossRef Medline