A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila

All animals exhibit innate behaviours in response to specific sensory stimuli that are likely to result from the activation of developmentally programmed neural circuits. Here we observe that Drosophila exhibit robust avoidance to odours released by stressed flies. Gas chromatography and mass spectrometry identifies one component of this ‘Drosophila stress odorant (dSO)’ as CO2. CO2 elicits avoidance behaviour, at levels as low as 0.1%. We used two-photon imaging with the Ca2+-sensitive fluorescent protein G-CaMP to map the primary sensory neurons governing avoidance to CO2. CO2 activates only a single glomerulus in the antennal lobe, the V glomerulus; moreover, this glomerulus is not activated by any of 26 other odorants tested. Inhibition of synaptic transmission in sensory neurons that innervate the V glomerulus, using a temperature-sensitive Shibire gene (Shits), blocks the avoidance response to CO2. Inhibition of synaptic release in the vast majority of other olfactory receptor neurons has no effect on this behaviour. These data demonstrate that the activation of a single population of sensory neurons innervating one glomerulus is responsible for an innate avoidance behaviour in Drosophila.

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

[2]  Dr. R. L. Desjardins,et al.  Advances in Bioclimatology 1 , 1992, Advances in Bioclimatology.

[3]  Ann-Shyn Chiang,et al.  Blockade of Neurotransmission in Drosophila Mushroom Bodies Impairs Odor Attraction, but Not Repulsion , 2003, Current Biology.

[4]  G. Stange,et al.  Carbon‐dioxide sensing structures in terrestrial arthropods , 1999, Microscopy research and technique.

[5]  M. Carlsson,et al.  Olfactory activation patterns in the antennal lobe of the sphinx moth, Manduca sexta , 2003, Journal of Comparative Physiology A.

[6]  Cornelia I Bargmann,et al.  Reprogramming Chemotaxis Responses: Sensory Neurons Define Olfactory Preferences in C. elegans , 1997, Cell.

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

[8]  M. Enserink What Mosquitoes Want: Secrets of Host Attraction , 2002, Science.

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

[10]  John R. Carlson,et al.  Odor Coding in the Drosophila Antenna , 2001, Neuron.

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

[12]  R. Menzel,et al.  The glomerular code for odor representation is species specific in the honeybee Apis mellifera , 1999, Nature Neuroscience.

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

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

[15]  F. Bogner,et al.  CO2 sensitive receptors on labial palps ofRhodogastria moths (Lepidoptera: Arctiidae): physiology, fine structure and central projection , 1986, Journal of Comparative Physiology A.

[16]  J. Hildebrand,et al.  An accessory olfactory pathway in Lepidoptera: the labial pit organ and its central projections in Manduca sexta and certain other sphinx moths and silk moths , 1986, Cell and Tissue Research.

[17]  R. Stocker,et al.  A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[19]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[20]  J. Hildebrand,et al.  Distinct projections of two populations of olfactory receptor axons in the antennal lobe of the sphinx moth Manduca sexta. , 1995, Chemical senses.

[21]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

[22]  S. Anton Central olfactory pathways in mosquitoes and other insects. , 1996, Ciba Foundation symposium.

[23]  T. Kitamoto Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. , 2001, Journal of neurobiology.

[24]  Bill S Hansson,et al.  Novel natural ligands for Drosophila olfactory receptor neurones , 2003, Journal of Experimental Biology.

[25]  Gilles Laurent,et al.  Transformation of Olfactory Representations in the Drosophila Antennal Lobe , 2004, Science.

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

[27]  H. Shorey Behavioral responses to insect pheromones. , 1973, Annual review of entomology.

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

[29]  G. Stange Sensory and Behavioural Responses of Terrestrial Invertebrates to Biogenic Carbon Dioxide Gradients , 1996 .

[30]  Y. Jan,et al.  dunce, a mutant of Drosophila deficient in learning. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

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

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