Chemosensory Coding by Neurons in the Coeloconic Sensilla of the Drosophila Antenna

Odor coding is based on the diverse sensitivities and response properties of olfactory receptor neurons (ORNs). In the Drosophila antenna, ORNs are housed in three major morphological types of sensilla. Although investigation of the Drosophila olfactory system has been expanding rapidly, the ORNs in one of these types, the coeloconic sensilla, have been essentially unexplored. We define four functional types of coeloconic sensilla through extracellular physiological recordings. Each type contains at least two neurons, with a total of at least seven distinct ORN classes that vary remarkably in their breadth of tuning. Analysis of 315 odorant–ORN combinations reveals how these neurons sample odor space via both excitation and inhibition. We identify a class of neurons that is narrowly tuned to small amines, and we find humidity detectors that define a cellular basis for hygroreception in Drosophila. The temporal dynamics of responses vary widely, enhancing the potential for complexity in the odor code. Molecular and genetic analysis shows that a broadly tuned ORN, antennal coeloconic 3B (ac3B), requires the odor receptor gene Or35a for its response in vivo. The activity of ac3B is not required for the response of the other ORN within that sensillum, ac3A. The functional analysis presented here, revealing a combination of highly specialized neurons and a broadly tuned ORN, along with the ancient origin of coeloconic sensilla, suggests that the specificities of these ORNs may reflect basic needs of an ancestral insect.

[1]  A. Dubin,et al.  Inactivation of olfactory sensilla of a single morphological type differentially affects the response of Drosophila to odors. , 2002, Journal of neurobiology.

[2]  K. Kaissling,et al.  Cell responses to single pheromone molecules may reflect the activation kinetics of olfactory receptor molecules , 2003, Journal of Comparative Physiology A.

[3]  H. Sass,et al.  Relationship between structure and function of antennal chemo-, hygro-, and thermoreceptive sensilla in Periplaneta americana , 1977, Cell and Tissue Research.

[4]  E. E. Davis,et al.  Ammonia-sensitive neurones on the first tarsi of the tick, Rhipicephalus sanguineus , 1980 .

[5]  S. van Straten,et al.  Volatile compounds in food. , 1977 .

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

[7]  H. Tichy,et al.  Low rates of change enhance effect of humidity on the activity of insect hygroreceptors , 2003, Journal of Comparative Physiology A.

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

[9]  B. Pophof.  Olfactory responses recorded from sensilla coeloconica of the silkmoth Bombyx mori , 1997 .

[10]  H. Altner,et al.  The structure of bimodal chemo-, thermo-, and hygroreceptive sensilla on the antenna of Locusta migratoria , 2004, Cell and Tissue Research.

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

[12]  John R. Carlson,et al.  Integrating the Molecular and Cellular Basis of Odor Coding in the Drosophila Antenna , 2003, Neuron.

[13]  J. Guillet,et al.  Shape and amplitude of the spikes induced by natural or electrical stimulation in insect receptors , 1972 .

[14]  S. Benzer,et al.  Behavioral genetics of thermosensation and hygrosensation in Drosophila. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[16]  R. Steinbrecht,et al.  Atlas of olfactory organs of Drosophila melanogaster , 1999 .

[17]  J. Carlson,et al.  Targeted Mutation of a Drosophila Odor Receptor Defines Receptor Requirement in a Novel Class of Sensillum , 2003, The Journal of Neuroscience.

[18]  E. Hallem,et al.  The odor coding system of Drosophila. , 2004, Trends in genetics : TIG.

[19]  A. Redkozubov.  High electrical resistance of the bombykol cell in an olfactory sensillum of Bombyx mori: Voltage- and current-clamp analysis , 1995 .

[20]  John R. Carlson,et al.  Coexpression of Two Functional Odor Receptors in One Neuron , 2005, Neuron.

[21]  John R. Carlson,et al.  Odorant response of individual sensilla on theDrosophila antenna , 1997, Invertebrate Neuroscience.

[22]  J. Thorson,et al.  Insect Olfactory Sensilla: Structural, Chemical and Electrical Aspects of the Functional Organisation , 1980 .

[23]  H Maarse,et al.  Volatile compounds in food : qualitative and quantitative data , 1990 .

[24]  W. Takken,et al.  The response of the malaria mosquito, Anopheles gambiae, to two components of human sweat, ammonia and l‐lactic acid, in an olfactometer , 2001 .

[25]  C. J. Otter,et al.  Odour sensitivity of antennal olfactory cells underlying grooved pegs of Anopheles gambiae s.s. and An. quadriannulatus , 2000 .

[26]  E. R. Rumbo.  The shape of extracellularly recorded nerve impulses from pheromone receptors , 1989 .

[27]  John R. Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Larva , 2005, Neuron.

[28]  J. Carlson,et al.  Candidate taste receptors in Drosophila. , 2000, Science.

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

[30]  John R Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Antenna , 2004, Cell.

[31]  R. Steinbrecht.  Pore structures in insect olfactory sensilla: A review of data and concepts , 1997 .

[32]  Peter J. Clyne,et al.  Odor Coding in a Model Olfactory Organ: TheDrosophila Maxillary Palp , 1999, The Journal of Neuroscience.

[33]  P. Guerin,et al.  Ammonia attracts the haematophagous bug Triatoma infestans : behavioural and neurophysiological data on nymphs , 1997, Journal of Comparative Physiology A.