Altered Representation of the Spatial Code for Odors after Olfactory Classical Conditioning Memory Trace Formation by Synaptic Recruitment

In the olfactory bulb of vertebrates or the homologous antennal lobe of insects, odor quality is represented by stereotyped patterns of neuronal activity that are reproducible within and between individuals. Using optical imaging to monitor synaptic activity in the Drosophila antennal lobe, we show here that classical conditioning rapidly alters the neural code representing the learned odor by recruiting new synapses into that code. Pairing of an odor-conditioned stimulus with an electric shock-unconditioned stimulus causes new projection neuron synapses to respond to the odor along with those normally activated prior to conditioning. Different odors recruit different groups of projection neurons into the spatial code. The change in odor representation after conditioning appears to be intrinsic to projection neurons. The rapid recruitment by conditioning of new synapses into the representation of sensory information may be a general mechanism underlying many forms of short-term memory.

[1]  C. D. Beck,et al.  Learning Performance of Normal and MutantDrosophila after Repeated Conditioning Trials with Discrete Stimuli , 2000, The Journal of Neuroscience.

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

[3]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[4]  Tim Tully,et al.  Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory , 2001, Nature.

[5]  L. Luo,et al.  Representation of the Glomerular Olfactory Map in the Drosophila Brain , 2002, Cell.

[6]  Ronald L. Davis,et al.  Drosophila fasciclinII Is Required for the Formation of Odor Memories and for Normal Sensitivity to Alcohol , 2001, Cell.

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

[8]  W. Gao,et al.  Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears , 2000, Nature Neuroscience.

[9]  R. Davis,et al.  Biochemistry of insect learning: lessons from bees and flies. , 1996, Insect biochemistry and molecular biology.

[10]  R. Menzel Searching for the memory trace in a mini-brain, the honeybee. , 2001, Learning & memory.

[11]  L. Squire Memory and Brain , 1987 .

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

[13]  A. Chess,et al.  Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe , 2000, Nature Neuroscience.

[14]  G. Laurent,et al.  Odor encoding as an active, dynamical process: experiments, computation, and theory. , 2001, Annual review of neuroscience.

[15]  Peter Mombaerts,et al.  How smell develops , 2001, Nature Neuroscience.

[16]  R H Hruban,et al.  Three-dimensional reconstruction of the human body. , 1988, AJR. American journal of roentgenology.

[17]  G. Laurent,et al.  Short-term memory in olfactory network dynamics , 1999, Nature.

[18]  M. T. Shipley,et al.  Centre–surround inhibition among olfactory bulb glomeruli , 2003, Nature.

[19]  R. Friedrich,et al.  Combinatorial and Chemotopic Odorant Coding in the Zebrafish Olfactory Bulb Visualized by Optical Imaging , 1997, Neuron.

[20]  J. Hildebrand,et al.  Synaptic organization of the uniglomerular projection neurons of the antennal lobe of the moth Manduca sexta: A laser scanning confocal and electron microscopic study , 1997, The Journal of comparative neurology.

[21]  Ronald L. Davis,et al.  P{Switch}, a system for spatial and temporal control of gene expression in Drosophila melanogaster , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Reinhard F. Stocker,et al.  The organization of the chemosensory system in Drosophila melanogaster: a rewiew , 2004, Cell and Tissue Research.

[23]  P. Hiesinger,et al.  Three‐dimensional reconstruction of the antennal lobe in Drosophila melanogaster , 1999, The Journal of comparative neurology.

[24]  Richard Axel,et al.  An Olfactory Sensory Map in the Fly Brain , 2000, Cell.

[25]  Andrey Rzhetsky,et al.  A Chemosensory Gene Family Encoding Candidate Gustatory and Olfactory Receptors in Drosophila , 2001, Cell.

[26]  M Heisenberg,et al.  Localization of a short-term memory in Drosophila. , 2000, Science.

[27]  A. Carleton,et al.  A dendrodendritic reciprocal synapse provides a recurrent excitatory connection in the olfactory bulb , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Ronald L. Davis Mushroom bodies and drosophila learning , 1993, Neuron.

[29]  Roberto Malinow,et al.  Genetic Manipulation of the Odor-Evoked Distributed Neural Activity in the Drosophila Mushroom Body , 2001, Neuron.

[30]  L. Vosshall Olfaction in Drosophila , 2000, Current Opinion in Neurobiology.

[31]  R. Davis,et al.  New series of Drosophila expression vectors suitable for behavioral rescue. , 1999, BioTechniques.

[32]  Gero Miesenböck,et al.  Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins , 1998, Nature.

[33]  R. Menzel,et al.  Representations of odours and odour mixtures visualized in the honeybee brain , 1997, Nature.

[34]  Ronald L. Davis,et al.  An Adjustable-threshold Algorithm for the Identification of Objects in Three-dimensional Images , 2003, Bioinform..

[35]  A. Chess,et al.  Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. , 1999, Genomics.

[36]  R. Nicoll,et al.  Synaptic plasticity and dynamic modulation of the postsynaptic membrane , 2000, Nature Neuroscience.

[37]  L. C. Katz,et al.  Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb , 1999, Neuron.

[38]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

[39]  R. Stocker,et al.  Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. , 1997, Journal of neurobiology.

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

[41]  A. Correspondent,et al.  Genetic manipulation , 1974, Nature.

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

[43]  Liqun Luo,et al.  Target neuron prespecification in the olfactory map of Drosophila , 2001, Nature.

[44]  Ronald L. Davis,et al.  Molecular biology and anatomy of Drosophila olfactory associative learning , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

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

[46]  Derek Lessing,et al.  Chemosensory behavior: the path from stimulus to response , 1999, Current Opinion in Neurobiology.

[47]  Richard Axel,et al.  Spatial Representation of the Glomerular Map in the Drosophila Protocerebrum , 2002, Cell.

[48]  J S Kauer,et al.  Imaging and coding in the olfactory system. , 2001, Annual review of neuroscience.