 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
The Journal of Neuroscience, November 19, 2003, 23(33):10495-10502
Previous Article | Next Article
Behavioral/Systems/Cognitive
Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila
Martin Schwaerzel,1 Maria Monastirioti,2 Henrike Scholz,1 Florence Friggi-Grelin,3 Serge Birman,3 andMartin Heisenberg1 1Lehrstuhl für Genetik und Neurobiologie, Biozentrum, Am Hubland, D-97074 Würzburg, Germany, 2Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology, 71110 Heraklion, Greece, and 3Developmental Biology Institute of Marseille, F-13288 Marseille Cedex 9, France.
The catecholamines play a major role in the regulation of behavior. Here we investigate, in the fly Drosophila melanogaster, the role of dopamine and octopamine (the presumed arthropod homolog of norepinephrine) during the formation of appetitive and aversive olfactory memories. We find that for the formation of both types of memories, cAMP signaling is necessary and sufficient within the same subpopulation of mushroom-body intrinsic neurons. On the other hand, memory formation can be distinguished by the requirement for different catecholamines, dopamine for aversive and octopamine for appetitive conditioning. Our results suggest that in associative conditioning, different memories are formed of the same odor under different circumstances, and that they are linked to the respective motivational systems by their specific modulatory pathways.
Key words: learning and memory; dopamine; octopamine; reinforcement; Drosophila; memory trace; synaptic plasticity
Received Aug 10, 2003; revised September 16, 2003; accepted September 23, 2003.
This article has been cited by other articles:
A. Yarali, S. Ehser, F. Z. Hapil, J. Huang, and B. Gerber
Odour intensity learning in fruit flies
Proc R Soc B, October 7, 2009; 276(1672): 3413 - 3420.
[Abstract] [Full Text] [PDF]
J. Carcaud, E. Roussel, M. Giurfa, and J.-C. Sandoz
Odour aversion after olfactory conditioning of the sting extension reflex in honeybees
J. Exp. Biol., March 1, 2009; 212(5): 620 - 626.
[Abstract] [Full Text] [PDF]
X. Liu, M. E. Buchanan, K.-A. Han, and R. L. Davis
The GABAA Receptor RDL Suppresses the Conditioned Stimulus Pathway for Olfactory Learning
J. Neurosci., February 4, 2009; 29(5): 1573 - 1579.
[Abstract] [Full Text] [PDF]
K. Honjo and K. Furukubo-Tokunaga
Distinctive Neuronal Networks and Biochemical Pathways for Appetitive and Aversive Memory in Drosophila Larvae
J. Neurosci., January 21, 2009; 29(3): 852 - 862.
[Abstract] [Full Text] [PDF]
A. B. Barron, R. Maleszka, P. G. Helliwell, and G. E. Robinson
Effects of cocaine on honey bee dance behaviour
J. Exp. Biol., January 15, 2009; 212(2): 163 - 168.
[Abstract] [Full Text] [PDF]
H. Zhao, X. Zheng, X. Yuan, L. Wang, X. Wang, Y. Zhong, Z. Xie, and T. Tully
ben Functions with Scamp during Synaptic Transmission and Long-Term Memory Formation in Drosophila
J. Neurosci., January 14, 2009; 29(2): 414 - 424.
[Abstract] [Full Text] [PDF]
K. G. Iliadi, A. Avivi, N. N. Iliadi, D. Knight, A. B. Korol, E. Nevo, P. Taylor, M. F. Moran, N. G. Kamyshev, and G. L. Boulianne
nemy encodes a cytochrome b561 that is required for Drosophila learning and memory
PNAS, December 16, 2008; 105(50): 19986 - 19991.
[Abstract] [Full Text] [PDF]
P. Masek and M. Heisenberg
Distinct memories of odor intensity and quality in Drosophila
PNAS, October 14, 2008; 105(41): 15985 - 15990.
[Abstract] [Full Text] [PDF]
K. Aoki, K. Kosakai, and M. Yoshino
Monoaminergic Modulation of the Na+-Activated K+ Channel in Kenyon Cells Isolated From the Mushroom Body of the Cricket (Gryllus bimaculatus) Brain
J Neurophysiol, September 1, 2008; 100(3): 1211 - 1222.
[Abstract] [Full Text] [PDF]
D. Sitaraman, M. Zars, H. LaFerriere, Y.-C. Chen, A. Sable-Smith, T. Kitamoto, G. E. Rottinghaus, and T. Zars
Serotonin is necessary for place memory in Drosophila
PNAS, April 8, 2008; 105(14): 5579 - 5584.
[Abstract] [Full Text] [PDF]
T. Yabumoto, F. Takanashi, Y. Kirino, and S. Watanabe
Nitric oxide is involved in appetitive but not aversive olfactory learning in the land mollusk Limax valentianus
Learn. Mem., April 2, 2008; 15(4): 229 - 232.
[Abstract] [Full Text] [PDF]
H. LaFerriere, D. J. Guarnieri, D. Sitaraman, S. Diegelmann, U. Heberlein, and T. Zars
Genetic Dissociation of Ethanol Sensitivity and Memory Formation in Drosophila melanogaster
Genetics, April 1, 2008; 178(4): 1895 - 1902.
[Abstract] [Full Text] [PDF]
C.-h. Yang, P. Belawat, E. Hafen, L. Y. Jan, and Y.-N. Jan
Drosophila Egg-Laying Site Selection as a System to Study Simple Decision-Making Processes
Science, March 21, 2008; 319(5870): 1679 - 1683.
[Abstract] [Full Text] [PDF]
M. J. Krashes and S. Waddell
Rapid Consolidation to a radish and Protein Synthesis-Dependent Long-Term Memory after Single-Session Appetitive Olfactory Conditioning in Drosophila
J. Neurosci., March 19, 2008; 28(12): 3103 - 3113.
[Abstract] [Full Text] [PDF]
B. Brembs, F. Christiansen, H. J. Pfluger, and C. Duch
Flight Initiation and Maintenance Deficits in Flies with Genetically Altered Biogenic Amine Levels
J. Neurosci., October 10, 2007; 27(41): 11122 - 11131.
[Abstract] [Full Text] [PDF]
A. S. Thum, A. Jenett, K. Ito, M. Heisenberg, and H. Tanimoto
Multiple Memory Traces for Olfactory Reward Learning in Drosophila
J. Neurosci., October 10, 2007; 27(41): 11132 - 11138.
[Abstract] [Full Text] [PDF]
S. Decker, S. McConnaughey, and T. L. Page
Circadian regulation of insect olfactory learning
PNAS, October 2, 2007; 104(40): 15905 - 15910.
[Abstract] [Full Text] [PDF]
T. Farooqui
Octopamine-Mediated Neuronal Plasticity in Honeybees: Implications for Olfactory Dysfunction in Humans
Neuroscientist, August 1, 2007; 13(4): 304 - 322.
[Abstract] [PDF]
V. Vergoz, H. A. Schreurs, and A. R. Mercer
Queen Pheromone Blocks Aversive Learning in Young Worker Bees
Science, July 20, 2007; 317(5836): 384 - 386.
[Abstract] [Full Text] [PDF]
Y.-C. Kim, H.-G. Lee, and K.-A. Han
D1 Dopamine Receptor dDA1 Is Required in the Mushroom Body Neurons for Aversive and Appetitive Learning in Drosophila
J. Neurosci., July 18, 2007; 27(29): 7640 - 7647.
[Abstract] [Full Text] [PDF]
K. Jorgensen, M. Stranden, J.-C. Sandoz, R. Menzel, and H. Mustaparta
Effects of two bitter substances on olfactory conditioning in the moth Heliothis virescens
J. Exp. Biol., July 15, 2007; 210(14): 2563 - 2573.
[Abstract] [Full Text] [PDF]
I. T. Barbarossa, P. Muroni, M. D. Setzu, and A. M. Angioy
Dose-Dependent Nonassociative Olfactory Learning in a Fly
Chem Senses, July 1, 2007; 32(6): 535 - 541.
[Abstract] [Full Text] [PDF]
K. Zhang, J. Z. Guo, Y. Peng, W. Xi, and A. Guo
Dopamine-Mushroom Body Circuit Regulates Saliency-Based Decision-Making in Drosophila
Science, June 29, 2007; 316(5833): 1901 - 1904.
[Abstract] [Full Text] [PDF]
S. F. Acevedo, E. I. Froudarakis, A. Kanellopoulos, and E. M.C. Skoulakis
Protection from premature habituation requires functional mushroom bodies in Drosophila
Learn. Mem., May 10, 2007; 14(5): 376 - 384.
[Abstract] [Full Text] [PDF]
K. R. Kaun, T. Hendel, B. Gerber, and M. B. Sokolowski
Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase
Learn. Mem., May 3, 2007; 14(5): 342 - 349.
[Abstract] [Full Text] [PDF]
S. J. Certel, M. G. Savella, D. C. F. Schlegel, and E. A. Kravitz
Modulation of Drosophila male behavioral choice
PNAS, March 13, 2007; 104(11): 4706 - 4711.
[Abstract] [Full Text] [PDF]
K. T. Beggs, K. A. Glendining, N. M. Marechal, V. Vergoz, I. Nakamura, K. N. Slessor, and A. R. Mercer
Queen pheromone modulates brain dopamine function in worker honey bees
PNAS, February 13, 2007; 104(7): 2460 - 2464.
[Abstract] [Full Text] [PDF]
M. Schwaerzel, A. Jaeckel, and U. Mueller
Signaling at A-Kinase Anchoring Proteins Organizes Anesthesia-Sensitive Memory in Drosophila
J. Neurosci., January 31, 2007; 27(5): 1229 - 1233.
[Abstract] [Full Text] [PDF]
A. B. Barron, R. Maleszka, R. K. Vander Meer, and G. E. Robinson
Octopamine modulates honey bee dance behavior
PNAS, January 30, 2007; 104(5): 1703 - 1707.
[Abstract] [Full Text] [PDF]
K. Foltenyi, R. Andretic, J. W. Newport, and R. J. Greenspan
Neurohormonal and Neuromodulatory Control of Sleep in Drosophila
Cold Spring Harb Symp Quant Biol, January 1, 2007; 72(0): 565 - 571.
[Abstract] [PDF]
B. Gerber and R. F. Stocker
The Drosophila Larva as a Model for Studying Chemosensation and Chemosensory Learning: A Review
Chem Senses, January 1, 2007; 32(1): 65 - 89.
[Abstract] [Full Text] [PDF]
H. Gu and D. K. O'Dowd
Cholinergic Synaptic Transmission in Adult Drosophila Kenyon Cells In Situ
J. Neurosci., January 4, 2006; 26(1): 265 - 272.
[Abstract] [Full Text] [PDF]
S. Diegelmann, M. Zars, and T. Zars
Genetic dissociation of acquisition and memory strength in the heat-box spatial learning paradigm in Drosophila
Learn. Mem., January 1, 2006; 13(1): 72 - 83.
[Abstract] [Full Text] [PDF]
M. Araki, T. Nagayama, and J. Sprayberry
Cyclic AMP Mediates Serotonin-Induced Synaptic Enhancement of Lateral Giant Interneuron of the Crayfish
J Neurophysiol, October 1, 2005; 94(4): 2644 - 2652.
[Abstract] [Full Text] [PDF]
T. Nisimura, A. Seto, K. Nakamura, M. Miyama, T. Nagao, S. Tamotsu, R. Yamaoka, and M. Ozaki
Experiential Effects of Appetitive and Nonappetitive Odors on Feeding Behavior in the Blowfly, Phormia regina: A Putative Role for Tyramine in Appetite Regulation
J. Neurosci., August 17, 2005; 25(33): 7507 - 7516.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|