Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age.

The olfactory system of several holometabolous insect species undergoes anatomical changes after eclosion of the imago, following those occurring during metamorphosis. In parallel, odor experience and learning performance also evolve with age. Here, we analyze the case of adult Drosophila females. Synaptogenesis in the antennal lobe (AL) starts in late pupa and continues during the first days of adult life, at the same time as the behavioral response to odors matures. Individual olfactory glomeruli (DM6, DM2, and V) display specific growth patterns between days 1 and 12 of adult life. Experience can modify the olfactory pathway both structurally and functionally as shown by adaptation experiments. The modifications associated with this form of nonassociative learning seem to take place at a critical age. Exposure to benzaldehyde at days 2-5 of adult life, but not at 8-11, causes behavioral adaptation as well as structural changes in DM2 and V glomeruli. Altered levels in intracellular cAMP, caused by dunce and rutabaga mutants, do not affect the normal changes in glomerular size, at least at day 6 of development, but they prevent those elicited by experience, establishing a molecular difference between glomerular changes of intrinsic versus environmental origin. Taken together, these data demonstrate an imprinting-like phenomenon in the olfactory pathway of young Drosophila adults, and illustrate its glomerulus-specific dynamics.

[1]  M Heisenberg,et al.  Structural plasticity in the Drosophila brain , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  J. Jaenike.  Effects of early adult experience on host selection in insects: Some experimental and theoretical results , 2005, Journal of Insect Behavior.

[3]  D. Laloi,et al.  Olfactory information transfer in the honeybee: compared efficiency of classical conditioning and early exposure , 2000, Animal Behaviour.

[4]  Gene E. Robinson,et al.  Experience- and Age-Related Outgrowth of Intrinsic Neurons in the Mushroom Bodies of the Adult Worker Honeybee , 2001, The Journal of Neuroscience.

[5]  A. Barron,et al.  Preimaginal conditioning in Drosophila revisited , 1999, Animal Behaviour.

[6]  Daniel R. Papaj,et al.  ECOLOGICAL AND EVOLUTIONARY ASPECTS OF LEARNING IN PHYTOPHAGOUS INSECTS , 1989 .

[7]  Hölldobler,et al.  Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus , 1996, The Journal of experimental biology.

[8]  A. Mercer,et al.  Activity-Dependent Changes to the Brain and Behavior of the Honey Bee, Apis mellifera (L.) , 1997, The Journal of Neuroscience.

[9]  Á. Acebes,et al.  Increasing the Number of Synapses Modifies Olfactory Perception in Drosophila , 2001, The Journal of Neuroscience.

[10]  J. Devaud,et al.  Odor Exposure Causes Central Adaptation and Morphological Changes in Selected Olfactory Glomeruli in Drosophila , 2001, The Journal of Neuroscience.

[11]  M Heisenberg,et al.  Vision affects mushroom bodies and central complex in Drosophila melanogaster. , 1997, Learning & memory.

[12]  T. Alloway.  Learning and Memory in Insects , 1972 .

[13]  J. Dubnau,et al.  Gene discovery in Drosophila: new insights for learning and memory. , 1998, Annual review of neuroscience.

[14]  I A Meinertzhagen,et al.  Experience-Dependent Developmental Plasticity in the Optic Lobe of Drosophila melanogaster , 1997, The Journal of Neuroscience.

[15]  A. Dubin,et al.  Voltage-activated and odor-modulated conductances in olfactory neurons of Drosophila melanogaster. , 1997, Journal of neurobiology.

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

[17]  W. Hershberger,et al.  Conditioning in Drosophila melanogaster. , 1967, Animal behaviour.

[18]  S. Corbet.  Insect chemosensory responses: a chemical legacy hypothesis , 1985 .

[19]  J. Carlson,et al.  Development and organization of the Drosophila olfactory system: an analysis using enhancer traps. , 1992, Journal of neurobiology.

[20]  R. Napper,et al.  Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee , 1996, The Journal of comparative neurology.

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

[22]  L. Tolbert,et al.  Glial cells stabilize axonal protoglomeruli in the developing olfactory lobe of the moth Manduca sexta , 1996, The Journal of comparative neurology.

[23]  R. Stocker,et al.  Larval chemosensory projections and invasion of adult afferents in the antennal lobe of Drosophila. , 1997, Journal of neurobiology.

[24]  C. Strambi,et al.  Neural Plasticity in the Adult Insect Brain and Its Hormonal Control , 1999 .

[25]  D. Jhaveri,et al.  Mechanisms underlying olfactory neuronal connectivity in Drosophila-the atonal lineage organizes the periphery while sensory neurons and glia pattern the olfactory lobe. , 2000, Developmental biology.

[26]  M. Breed,et al.  Honey bee, Apis mellifera, nestmate discrimination: hydrocarbon effects and the evolutionary implications of comb choice , 1992, Animal Behaviour.

[27]  R. Stocker,et al.  Anatomical and neurochemical classification of the antennal glomeruli in Drosophila melanogaster meigen (Diptera : Drosophilidae) , 1988 .

[28]  B. Rogina,et al.  Changes in gene expression during post-eclosional development in the olfactory system of Drosophila melanogaster , 1995, Mechanisms of Development.

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