Insect olfactory memory in time and space

Recent studies using functional optical imaging have revealed that cellular memory traces form in different areas of the insect brain after olfactory classical conditioning. These traces are revealed as increased calcium signals or synaptic release from defined neurons, and include a short-lived trace that forms immediately after conditioning in antennal lobe projection neurons, an early trace in dopaminergic neurons, and a medium-term trace in dorsal paired medial neurons. New molecular genetic tools have revealed that for normal behavioral memory performance, synaptic transmission from the mushroom body neurons is required only during retrieval, whereas synaptic transmission from dopaminergic neurons is required at the time of acquisition and synaptic transmission from dorsal paired medial neurons is required during the consolidation period. Such experimental results are helping to identify the types of neurons that participate in olfactory learning and when their participation is required. Olfactory learning often occurs alongside crossmodal interactions of sensory information from other modalities. Recent studies have revealed complex interactions between the olfactory and the visual senses that can occur during olfactory learning, including the facilitation of learning about subthreshold olfactory stimuli due to training with concurrent visual stimuli.

[1]  U. Müller Prolonged Activation of cAMP-Dependent Protein Kinase during Conditioning Induces Long-Term Memory in Honeybees , 2000, Neuron.

[2]  Eugene Berezikov,et al.  Crossmodal Interactions Between Olfactory and Visual Learning in Drosophila , 2005 .

[3]  M. Heisenberg,et al.  Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila , 2003, The Journal of Neuroscience.

[4]  Ronald L. Davis,et al.  Gene expression systems in Drosophila: a synthesis of time and space. , 2004, Trends in genetics : TIG.

[5]  Ronald L. Davis,et al.  Detection of Calcium Transients in DrosophilaMushroom Body Neurons with Camgaroo Reporters , 2003, The Journal of Neuroscience.

[6]  M. Srinivasan,et al.  The concepts of ‘sameness’ and ‘difference’ in an insect , 2001, Nature.

[7]  A. Fiala,et al.  Genetically Expressed Cameleon in Drosophila melanogaster Is Used to Visualize Olfactory Information in Projection Neurons , 2002, Current Biology.

[8]  Mandyam V Srinivasan,et al.  Floral scents induce recall of navigational and visual memories in honeybees , 2004, Journal of Experimental Biology.

[9]  J. Hildebrand,et al.  Learning modulates the ensemble representations for odors in primary olfactory networks. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[10]  W. Quinn,et al.  The amnesiac Gene Product Is Expressed in Two Neurons in the Drosophila Brain that Are Critical for Memory , 2000, Cell.

[11]  W. Quinn,et al.  The Drosophila memory mutant amnesiac , 1979, Nature.

[12]  Ronald L. Davis,et al.  Drosophila DPM Neurons Form a Delayed and Branch-Specific Memory Trace after Olfactory Classical Conditioning , 2005, Cell.

[13]  Ronald L. Davis,et al.  Olfactory memory formation in Drosophila: from molecular to systems neuroscience. , 2005, Annual review of neuroscience.

[14]  Michael J. Krashes,et al.  Drosophila Dorsal Paired Medial Neurons Provide a General Mechanism for Memory Consolidation , 2006, Current Biology.

[15]  M. Low,et al.  Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory , 2022 .

[16]  Karel Svoboda,et al.  Stereotyped Odor-Evoked Activity in the Mushroom Body of Drosophila Revealed by Green Fluorescent Protein-Based Ca2+ Imaging , 2004, The Journal of Neuroscience.

[17]  Ronald L. Davis,et al.  Thirty years of olfactory learning and memory research in Drosophila melanogaster , 2005, Progress in Neurobiology.

[18]  R. Davis,et al.  The Role of Drosophila Mushroom Body Signaling in Olfactory Memory , 2001, Science.

[19]  J. B. Duffy,et al.  GAL4 system in drosophila: A fly geneticist's swiss army knife , 2002, Genesis.

[20]  T. Sejnowski,et al.  Fast Odor Learning Improves Reliability of Odor Responses in the Locust Antennal Lobe , 2005, Neuron.

[21]  Gerald M. Rubin,et al.  Localization of Long-Term Memory Within the Drosophila Mushroom Body , 2001 .

[22]  Ronald L. Davis,et al.  Spatiotemporal Rescue of Memory Dysfunction in Drosophila , 2003, Science.

[23]  Gero Miesenböck,et al.  Transmission of Olfactory Information between Three Populations of Neurons in the Antennal Lobe of the Fly , 2002, Neuron.

[24]  S. Waddell,et al.  Diverse Odor-Conditioned Memories Require Uniquely Timed Dorsal Paired Medial Neuron Output , 2004, Neuron.

[25]  Ronald L. Davis,et al.  Altered Representation of the Spatial Code for Odors after Olfactory Classical Conditioning Memory Trace Formation by Synaptic Recruitment , 2004, Neuron.

[26]  G. Roman,et al.  G(o) signaling is required for Drosophila associative learning , 2006, Nature Neuroscience.

[27]  A. Fiala,et al.  Punishment Prediction by Dopaminergic Neurons in Drosophila , 2005, Current Biology.

[28]  A. Wong,et al.  Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain , 2003, Cell.

[29]  Ronald L. Davis,et al.  Pharmacogenetic rescue in time and space of the rutabaga memory impairment by using Gene-Switch , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Menzel,et al.  Associative learning modifies neural representations of odors in the insect brain , 1999, Nature Neuroscience.