Random Convergence of Olfactory Inputs in the Drosophila Mushroom Body

The mushroom body in the fruitfly Drosophila melanogaster is an associative brain centre that translates odour representations into learned behavioural responses. Kenyon cells, the intrinsic neurons of the mushroom body, integrate input from olfactory glomeruli to encode odours as sparse distributed patterns of neural activity. We have developed anatomic tracing techniques to identify the glomerular origin of the inputs that converge onto 200 individual Kenyon cells. Here we show that each Kenyon cell integrates input from a different and apparently random combination of glomeruli. The glomerular inputs to individual Kenyon cells show no discernible organization with respect to their odour tuning, anatomic features or developmental origins. Moreover, different classes of Kenyon cells do not seem to preferentially integrate inputs from specific combinations of glomeruli. This organization of glomerular connections to the mushroom body could allow the fly to contextualize novel sensory experiences, a feature consistent with the role of this brain centre in mediating learned olfactory associations and behaviours.

[1]  M Heisenberg,et al.  Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. , 1994, Science.

[2]  Tim Tully,et al.  Associative Learning Disrupted by Impaired Gs Signaling in Drosophila Mushroom Bodies , 1996, Science.

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

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

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

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

[7]  I. Meinertzhagen,et al.  Synaptic organization of the mushroom body calyx in Drosophila melanogaster , 2002, The Journal of comparative neurology.

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

[9]  M. Heisenberg Mushroom body memoir: from maps to models , 2003, Nature Reviews Neuroscience.

[10]  Holger Kessler,et al.  Maps to models , 2004 .

[11]  Devanand S. Manoli,et al.  Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour , 2005, Nature.

[12]  D. Kvitsiani,et al.  Neural Circuitry that Governs Drosophila Male Courtship Behavior , 2005, Cell.

[13]  John R. Carlson,et al.  Coding of Odors by a Receptor Repertoire , 2006, Cell.

[14]  Ann-Shyn Chiang,et al.  A Map of Olfactory Representation in the Drosophila Mushroom Body , 2007, Cell.

[15]  L. Luo,et al.  Comprehensive Maps of Drosophila Higher Olfactory Centers: Spatially Segregated Fruit and Pheromone Representation , 2007, Cell.

[16]  L. Vosshall,et al.  Molecular architecture of smell and taste in Drosophila. , 2007, Annual review of neuroscience.

[17]  Kei Ito,et al.  Neuronal assemblies of the Drosophila mushroom body , 2008, The Journal of comparative neurology.

[18]  Glenn C. Turner,et al.  Olfactory representations by Drosophila mushroom body neurons. , 2008, Journal of neurophysiology.

[19]  C. Lehner,et al.  Cell-Type-Specific TEV Protease Cleavage Reveals Cohesin Functions in Drosophila Neurons , 2008, Developmental cell.

[20]  Gilles Laurent,et al.  Testing Odor Response Stereotypy in the Drosophila Mushroom Body , 2008, Neuron.

[21]  Gaia Tavosanis,et al.  Synaptic organization in the adult Drosophila mushroom body calyx , 2009, The Journal of comparative neurology.

[22]  Yoshinori Aso,et al.  The Mushroom Body of Adult Drosophila Characterized by GAL4 Drivers , 2009, Journal of neurogenetics.

[23]  Richard Axel,et al.  A dimorphic pheromone circuit in Drosophila from sensory input to descending output , 2010, Nature.

[24]  Yisheng He,et al.  A Complete Developmental Sequence of a Drosophila Neuronal Lineage as Revealed by Twin-Spot MARCM , 2010, PLoS biology.

[25]  G. Rubin,et al.  Mushroom body efferent neurons responsible for aversive olfactory memory retrieval in Drosophila , 2011, Nature Neuroscience.

[26]  Robert A. A. Campbell,et al.  Cellular-Resolution Population Imaging Reveals Robust Sparse Coding in the Drosophila Mushroom Body , 2011, The Journal of Neuroscience.

[27]  Charles S. Zuker,et al.  The Coding of Temperature in the Drosophila Brain , 2011, Cell.

[28]  Zhiyuan Lu,et al.  Different classes of input and output neurons reveal new features in microglomeruli of the adult Drosophila mushroom body calyx , 2012, The Journal of comparative neurology.

[29]  Jai Y. Yu,et al.  Dopamine neurons modulate pheromone responses in Drosophila courtship learning , 2012, Nature.