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Representation of binary pheromone blends by glomerulus-specific olfactory projection neurons

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Abstract

An outstanding challenge in olfactory neurobiology is to explain how glomerular networks encode information about stimulus mixtures, which are typical of natural olfactory stimuli. In the moth Manduca sexta, a species-specific blend of two sex-pheromone components is required for reproductive signaling. Each component stimulates a different population of olfactory receptor cells that in turn target two identified glomeruli in the macroglomerular complex of the male’s antennal lobe. Using intracellular recording and staining, we examined how responses of projection neurons innervating these glomeruli are modulated by changes in the level and ratio of the two essential components in stimulus blends. Compared to projection neurons specific for one component, projection neurons that integrated information about the blend (received excitatory input from one component and inhibitory input from the other) showed enhanced ability to track a train of stimulus pulses. The precision of stimulus-pulse tracking was furthermore optimized at a synthetic blend ratio that mimics the physiological response to an extract of the female’s pheromone gland. Optimal responsiveness of a projection neuron to repetitive stimulus pulses therefore appears to depend not only on stimulus intensity but also on the relative strength of the two opposing synaptic inputs that are integrated by macroglomerular complex projection neurons.

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Abbreviations

AL :

Antennal lobe

BAL :

Bombykal

C15 :

(E,Z)-11,13-pentadecadienal

MGC :

Macroglomerular complex

ORC :

Olfactory receptor cell

PN :

Projection neuron

T1 :

Toroid 1 glomerulus of the MGC

References

  • Almaas TJ, Christensen TA, Mustaparta H (1991) Chemical communication in heliothine moths. I. Antennal receptor neurons encode several features of intra- and interspecific odorants in the male corn earworm moth Helicoverpa zea. J Comp Physiol 169:259–274

    Google Scholar 

  • Anton S, Löfstedt C, Hansson BS (1997) Central nervous system processing of sex pheromones in two strains of the European Corn Borer Ostrinia nubilalis (Lepidoptera: Pyralidae). J Exp Biol 200:1073–1087

    CAS  PubMed  Google Scholar 

  • Arn H, Tóth M, Priesner E (1992) List of sex pheromones of Lepidoptera and related attractants. 2nd edn. International Organization for Biological Control, West Palearctic Regional Section, Montfavet, France

  • Baker TC (1989) Sex pheromone communication in the Lepidoptera: new research progress. Experientia 45:248–262

    CAS  Google Scholar 

  • Bell RA, Joachim FA (1976) Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am 69:365–373

    Google Scholar 

  • Boeckh J (1984) Neurophysiological aspects of insect olfaction. In: Lewis T (ed) Insect communication. Academic Press, Orlando, pp 83–104

    Google Scholar 

  • de Bruyne M, Foster K, Carlson JR (2000) Odor coding in the Drosophila antenna. Neuron 30:537–552

    Article  Google Scholar 

  • Christensen TA, Hildebrand JG (1987) Male-specific, sex-pheromone-selective projection neurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol A 160:553–569

    CAS  PubMed  Google Scholar 

  • Christensen TA, Hildebrand JG (1990) Representation of sex-pheromonal information in the insect brain. In: Døving KB (ed) ISOT X, Proceedings of the 10th international symposium on olfaction and taste. University of Oslo, Oslo, pp 142–150

  • Christensen TA, Hildebrand JG (1997) Coincident stimulation with pheromone components improves temporal pattern resolution in central olfactory neurons. J Neurophysiol 77:775–781

    CAS  PubMed  Google Scholar 

  • Christensen TA, Hildebrand JG (2002) Pheromonal and host-odor processing in the insect antennal lobe: how different? Curr Opin Neurobiol 12:393–399

    Article  CAS  PubMed  Google Scholar 

  • Christensen TA, White J (2000) Representation of olfactory information in the brain. In: Finger TE, Silver WL, Restrepo D (eds) The neurobiology of taste and smell, vol 2. Wiley-Liss, New York, pp 201–232

  • Christensen TA, Heinbockel T, Hildebrand JG (1996) Olfactory information processing in the brain: encoding chemical and temporal features of odors. J Neurobiol 30:82–91

    Article  CAS  PubMed  Google Scholar 

  • Christensen TA, Mustaparta H, Hildebrand JG (1989) Discrimination of sex pheromone blends in the olfactory system of the moth. Chem Senses 14:463–477

    CAS  Google Scholar 

  • Christensen TA, Waldrop BR, Hildebrand JG (1998) Multitasking in the olfactory system: context-dependent responses to odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons. J Neurosci 18:5999–6008

    CAS  PubMed  Google Scholar 

  • Christensen TA, Pawlowski VM, Lei H, Hildebrand JG (2000) Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles. Nat Neurosci 3:927–931

    Article  CAS  PubMed  Google Scholar 

  • Christensen TA, Harrow ID, Cuzzocrea C, Randolph PW, Hildebrand JG (1995) Distinct projections of two populations of olfactory receptor neurons in the antennal lobe of the sphinx moth Manduca sexta. Chem Senses 20:313–323

    CAS  PubMed  Google Scholar 

  • Christensen TA, Lei H, Hildebrand JG (2003) Coordination of cental odor representations through transient, non-oscillatory synchronization of glomerular output neurons. PNAS 100:11076–11081

    Article  CAS  PubMed  Google Scholar 

  • Friedrich RW, Stopfer M (2001) Recent dynamics in olfactory population coding. Curr Opin Neurobiol 11:468–474

    Article  CAS  PubMed  Google Scholar 

  • Galizia CG, Sachse S, Rappert A, Menzel R (1999) The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2:473–478

    Article  CAS  PubMed  Google Scholar 

  • Hansson BS, Christensen TA (1999) Functional characteristics of the antennal lobe. In: Hansson BS (ed) Insect olfaction. Springer, Berlin Heidelberg New York, pp 126–161

    Google Scholar 

  • Hansson BS, Christensen TA, Hildebrand JG (1991) Functionally distinct subdivisons of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta. J Comp Neurol 312:264–278

    CAS  PubMed  Google Scholar 

  • Heinbockel T, Christensen TA, Hildebrand JG (1995) Subunit architecture of the macroglomerular complex and the integrative function of output neurons in the moth, Manduca sexta. Chem Senses 20:707

    Google Scholar 

  • Heinbockel T, Christensen TA, Hildebrand JG (1999) Temporal tuning of odor responses in pheromone-responsive projection neurons in the brain of the sphinx moth Manduca sexta. J Comp Neurol 409:1–12

    Article  CAS  PubMed  Google Scholar 

  • Hildebrand JG (1996) Olfactory control of behavior in moths: central processing of odor information and the functional significance of olfactory glomeruli. J Comp Physiol A 178:5–19

    CAS  PubMed  Google Scholar 

  • Homberg U, Christensen TA, Hildebrand TA (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477–501

    Article  CAS  PubMed  Google Scholar 

  • Homberg U, Hoskins SG, Hildebrand JG (1995) Distribution of acetylcholinesterase activity in the deutocerebrum of the sphinx moth Manduca sexta. Cell Tissue Res 279:249–259

    Article  CAS  PubMed  Google Scholar 

  • Kaissling K-E (1996) Peripheral mechanisms of pheromone reception in moths. Chem Senses 21:257–268

    CAS  PubMed  Google Scholar 

  • Kaissling K-E, Hildebrand JG, Tumlinson JH (1989) Pheromone receptor cells in the male moth Manduca sexta. Arch Insect Biochem Physiol 10:273–279

    CAS  Google Scholar 

  • Keller A, Vosshall LB (2003) Decoding olfaction in Drosophila. Curr Opin Neurobiol 13:103–110

    Article  CAS  PubMed  Google Scholar 

  • Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD (2001) Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu Rev Neurosci 24:263–297

    Article  CAS  PubMed  Google Scholar 

  • Lei H, Christensen TA, Hildebrand JG (2002) Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci 5:557–565

    Article  CAS  PubMed  Google Scholar 

  • Leon M, Johnson BA (2003) Olfactory coding in the mammalian olfactory bulb. Brain Res Rev 42:23–32

    Article  PubMed  Google Scholar 

  • Murlis J (1997) Odor plumes and the signal they provide. In: Cardé RT, Minks AK (eds) Insect pheromone research—new directions. Chapman and Hall, New York, pp 221–231

    Google Scholar 

  • Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenböck G (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36:463–474

    Article  CAS  PubMed  Google Scholar 

  • Pichon Y, Sattelle DB, Lane NJ (1972) Conduction processes in the nerve cord of the moth Manduca sexta in relation to its ultrastructure and haemolymph ionic composition. J Exp Biol 56:717–734

    CAS  PubMed  Google Scholar 

  • Prescott DJ, Hildebrand JG, Sanes JR, Jewett S (1977) Biochemical and developmental studies of acetylcholine metabolism in the central nervous system of the moth Manduca sexta. Comp Biochem Physiol C 56:77–84

    Article  CAS  Google Scholar 

  • Reisenman CE, Christensen TA, Hildebrand JG (2004) Enantioselectivity of projection neurons innervating identified olfactory glomeruli. J Neurosci 24:2602–2611

    Article  CAS  PubMed  Google Scholar 

  • Sachse S, Galizia CG (2003) The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur J Neurosci 18:2119–2132

    Article  PubMed  Google Scholar 

  • Sanes JR, Hildebrand JG (1976) Structure and development of antennae in a moth, Manduca sexta. Dev Biol 51:282–299

    Google Scholar 

  • Stopfer M, Jayaramann V, Laurent G (2003) Intensity versus identity coding in an olfactory system. Neuron 39:991–1004

    Article  CAS  PubMed  Google Scholar 

  • Strausfeld NJ (1989) Cellular organization in male-specific olfactory neuropil in the moth Manduca sexta. In: Elsner N, Singer W (eds) Dynamics and plasticity in neuronal systems. Thieme, Stuttgart, p 79

    Google Scholar 

  • Sun XJ, Tolbert LP, Hildebrand JG (1993) Ramification pattern and ultrastructural characteristics of the serotonin immunoreactive neuron in the antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron microscopic study. J Comp Neurol 338:5–16

    CAS  PubMed  Google Scholar 

  • Tumlinson JH, Brennan MM, Doolittle RE, Mitchell ER, Brabham A, Mazomenos BE, Baumhover AH, Jackson DM (1989) Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel. Arch Insect Biochem Physiol 10:255–271

    CAS  Google Scholar 

  • Vickers NJ, Christensen TA, Baker TC, Hildebrand JG (2001) Odour-plume dynamics influence the brain’s olfactory code. Nature 410:466–470

    Article  CAS  PubMed  Google Scholar 

  • Wang JW, Wong AM, Flores J, Vosshall LB, Axel R (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271–282

    Article  CAS  PubMed  Google Scholar 

  • Wu W, Anton S, Löfstedt C, Hansson BS (1996) Discrimination among pheromone component blends by interneurons in male antennal lobes of two populations of the turnip moth, Agrotis segetum. PNAS 93:8022–8027

    Article  CAS  PubMed  Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, Englewood Cliffs

    Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Vonnie D.C. Shields for comments on the manuscript. We thank Dr. Rebecca Johnston and Dr. Vonnie D.C. Shields for advice on statistical analysis, Patricia Jansma and Wendy Pott for technical advice on confocal microscopy, Peggy Randolph for general laboratory assistance, Dr. A.A. Osman for insect rearing, and Dr. J.H. Tumlinson (USDA, Gainesville, Florida, USA) for synthetic compounds. This study was supported by a Flinn Foundation Biology Graduate Fellowship and a Sensory Science Scholarship to T.H. and NIH grants AI-23253 and DC-02751 to J.G.H. The experiments described in this study comply with the Principles of animal care, publication No. 86-23, revised 1985 of the National Institutes of Health and also with the current laws of the USA.

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Heinbockel, T., Christensen, T.A. & Hildebrand, J.G. Representation of binary pheromone blends by glomerulus-specific olfactory projection neurons. J Comp Physiol A 190, 1023–1037 (2004). https://doi.org/10.1007/s00359-004-0559-7

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