Essential Role of the Mushroom Body in Context-Dependent CO2 Avoidance in Drosophila

Internal state as well as environmental conditions influence choice behavior. The neural circuits underpinning state-dependent behavior remain largely unknown. Carbon dioxide (CO2) is an important olfactory cue for many insects, including mosquitoes, flies, moths, and honeybees [1]. Concentrations of CO2 higher than 0.02% above atmospheric level trigger a strong innate avoidance in the fly Drosophila melanogaster [2, 3]. Here, we show that the mushroom body (MB), a brain center essential for olfactory associative memories [4-6] but thought to be dispensable for innate odor processing [7], is essential for CO2 avoidance behavior only in the context of starvation or in the context of a food-related odor. Consistent with this, CO2 stimulation elicits Ca(2+) influx into the MB intrinsic cells (Kenyon cells: KCs) in vivo. We identify an atypical projection neuron (bilateral ventral projection neuron, biVPN) that connects CO2 sensory input bilaterally to the MB calyx. Blocking synaptic output of the biVPN completely abolishes CO2 avoidance in food-deprived flies, but not in fed flies. These findings show that two alternative neural pathways control innate choice behavior, and they are dependent on the animal's internal state. In addition, they suggest that, during innate choice behavior, the MB serves as an integration site for internal state and olfactory input.

[1]  L. Abbott,et al.  Random Convergence of Olfactory Inputs in the Drosophila Mushroom Body , 2013, Nature.

[2]  John R. Carlson,et al.  The molecular basis of CO2 reception in Drosophila , 2007, Proceedings of the National Academy of Sciences.

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

[4]  A. Fiala.  Olfaction and olfactory learning in Drosophila: recent progress , 2007, Current Opinion in Neurobiology.

[5]  H. L. Carson,et al.  The Genetics and Biology of Drosophila , 1976, Heredity.

[6]  Jing W. Wang,et al.  Presynaptic Facilitation by Neuropeptide Signaling Mediates Odor-Driven Food Search , 2011, Cell.

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

[8]  Guan-Yu Chen,et al.  Three-Dimensional Reconstruction of Brain-wide Wiring Networks in Drosophila at Single-Cell Resolution , 2011, Current Biology.

[9]  David J. Anderson,et al.  A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila , 2004, Nature.

[10]  Gyunghee Lee,et al.  Hemolymph Sugar Homeostasis and Starvation-Induced Hyperactivity Affected by Genetic Manipulations of the Adipokinetic Hormone-Encoding Gene in Drosophila melanogaster , 2004, Genetics.

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

[12]  R. Strauss,et al.  Behavioral consequences of dopamine deficiency in the Drosophila central nervous system , 2010, Proceedings of the National Academy of Sciences.

[13]  Julie H. Simpson,et al.  A GAL4-driver line resource for Drosophila neurobiology. , 2012, Cell reports.

[14]  T. Tanimura,et al.  Suppression of Conditioned Odor Approach by Feeding Is Independent of Taste and Nutritional Value in Drosophila , 2013, Current Biology.

[15]  Leslie B. Vosshall,et al.  Two chemosensory receptors together mediate carbon dioxide detection in Drosophila , 2007, Nature.

[16]  Kei Ito,et al.  Activity-Dependent Plasticity in an Olfactory Circuit , 2007, Neuron.

[17]  H. L. Carson,et al.  The genetics and biology of Drosophila. Vol. 3e. , 1986 .

[18]  G. Rubin,et al.  Refinement of Tools for Targeted Gene Expression in Drosophila , 2010, Genetics.

[19]  Manfred Forstreuter,et al.  Behavioral responses of Drosophila to biogenic levels of carbon dioxide depend on life-stage, sex and olfactory context , 2006, Journal of Experimental Biology.

[20]  J. Dubnau,et al.  Functional anatomy: From molecule to memory , 2001, Current Biology.

[21]  David J. Anderson,et al.  Light Activation of an Innate Olfactory Avoidance Response in Drosophila , 2007, Current Biology.

[22]  Jasper Akerboom,et al.  Optimization of a GCaMP Calcium Indicator for Neural Activity Imaging , 2012, The Journal of Neuroscience.

[23]  Anandasankar Ray,et al.  Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants , 2009, Nature.

[24]  André Fiala,et al.  In Vivo Calcium Imaging of Brain Activity in Drosophila by Transgenic Cameleon Expression , 2003, Science's STKE.

[25]  Cori Bargmann,et al.  GFP Reconstitution Across Synaptic Partners (GRASP) Defines Cell Contacts and Synapses in Living Nervous Systems , 2008, Neuron.

[26]  Barry J. Dickson,et al.  The Drosophila pheromone cVA activates a sexually dimorphic neural circuit , 2008, Nature.

[27]  Ronald L. Davis,et al.  Olfactory learning in Drosophila. , 2010, Physiology.

[28]  John G Hildebrand,et al.  Roles and effects of environmental carbon dioxide in insect life. , 2008, Annual review of entomology.

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

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

[31]  Shamik Dasgupta,et al.  A Neural Circuit Mechanism Integrating Motivational State with Memory Expression in Drosophila , 2009, Cell.

[32]  F Kidd,et al.  RESPIRATORY ACTIVITY AND DURATION OF LIFE OF APPLES GATHERED AT DIFFERENT STAGES OF DEVELOPMENT AND SUBSEQUENTLY MAINTAINED AT A CONSTANT TEMPERATURE. , 1945, Plant physiology.