Adaptive Processing in the Insect Olfactory System

  • Chapter
  • First Online:
The Ecology of Animal Senses

Abstract

Insects live in a complex olfactory environment containing thousands of volatile organic compounds (olfactory stimuli) at various intensities and mixture proportions, yet insects can detect and respond to specific olfactory stimuli at millisecond timescales. In this chapter, we describe the mechanisms by which the insect olfactory system can efficiently process an olfactory stimulus and how it filters the signal from background noise. Highlighting recent results from a variety of insect species, we consider: (1) the nature of the olfactory environment, (2) how olfactory information is filtered in the periphery, and (3) how the central nervous system efficiently and adaptively processes olfactory information. We propose that plasticity encoded in state- and learning-related processes allows the insect olfactory system to process and distinguish olfactory signals efficiently from background and to allow both the large-scale (e.g., meaning or value) and fine-scale (e.g., identity and composition) features of a stimulus to be encoded.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AL:

Antennal lobe

GABA:

γ-Aminobutyric acid

GC:

Gas chromatography

GC-EAD:

Gas chromatography coupled with electroantennographic detection

iLPN:

Interneuron in the lateral protocerebrum

LN:

Local interneuron

LP:

Lateral protocerebrum

MB:

Mushroom body

OBP:

Odorant binding protein

OR:

Olfactory receptor

ORC:

Olfactory receptor cell

PN:

Projection neuron

VOC:

Volatile organic compound

References

  • Acebes A, Martín-Peña A, Chevalier V, Ferrús A (2011) Synapse loss in olfactory local interneurons modifies perception. J Neurosci 31:2734–2745

    CAS  PubMed  Google Scholar 

  • Anton S, Homberg U (1999) Antennal lobe structure. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 97–124

    Google Scholar 

  • Arn H, Städler E, Rauscher S (1975) The electroantennographic detector—a selective and sensitive tool in the gas chromatographic analysis of insect pheromones. Z Naturforsch Sect C Biosci 30:722–725

    Google Scholar 

  • Ayasse M, Schiestl FP, Paulus HF, Löfstedt C, Hansson B, Ibarra F, Francke W (2000) Evolution of reproductive strategies in the sexually deceptive orchid Ophrys sphegodes: how does flower-specific variation of odor signals influence reproductive success? Evolution 54:1995–2006

    CAS  PubMed  Google Scholar 

  • Baker TC (2008) Balanced olfactory antagonism as a concept for understanding evolutionary shifts in moth sex pheromone blends. J Chem Ecol 34:971–981

    CAS  PubMed  Google Scholar 

  • Baker TC, Hansson BS, Löfstedt C, Löfqvist J (1988) Adaptation of antennal neurons in moths is associated with cessation of pheromone-mediated upwind flight. Proc Natl Acad Sci U S A 85:9826–9830

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bargmann CI (2006) Comparative chemosensation from receptors to ecology. Nature 444:295–301

    CAS  PubMed  Google Scholar 

  • Barrozo RB, Gadenne C, Anton S (2010) Switching attraction to inhibition: mating-induced reversed role of sex pheromone in an insect. J Exp Biol 213:2933–2939

    PubMed  Google Scholar 

  • Bau J, Justus KA, Loudon C, Cardé RT (2005) Electroantennographic resolution of pulsed pheromone plumes in two species of moths with bipectinate antennae. Chem Senses 30:771–780

    PubMed  Google Scholar 

  • Cardé RT, Willis M (2008) Navigational strategies used by insects to find distant, wind-borne sources of odor. J Chem Ecol 34:854–866

    PubMed  Google Scholar 

  • Chou Y, Spletter ML, Yaksi E, Leong JCS, Wilson RI, Luo L (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13:439–449

    CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen TA, Waldrop BR, Harrow ID, Hildebrand JG (1993) Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J Comp Physiol A 173:385–399

    CAS  PubMed  Google Scholar 

  • Clifford MR, Riffell JA (2013) Mixture and odorant processing in the olfactory systems of insects: a comparative perspective. J Comp Physiol A 199:911–928

    CAS  Google Scholar 

  • Conner WE, Eisner T, Vander Meer RK, Guerrero A, Ghiringelli D, Meinwald J (1980) Sex attractant of an arctiid moth (Utetheisa ornatrix): a pulsed chemical signal. Behav Ecol Sociobiol 7:55–63

    Google Scholar 

  • Dacks AM, Riffell JA, Martin JP, Gage SL, Nighorn AJ (2012) Olfactory modulation by dopamine in the context of aversive learning. J Neurophysiol 108:539–550

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daly KC, Christensen TA, Lei H, Smith BH, Hildebrand JG (2004) Learning modulates the ensemble representations for odors in primary olfactory networks. Proc Natl Acad Sci U S A 101:10476–10481

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Belle J, Heisenberg M (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692–695

    PubMed  Google Scholar 

  • De Bruyne M, Foster K, Carlson JR (2001) Odor coding in the Drosophila antenna. Neuron 30:537–552

    PubMed  Google Scholar 

  • Dekker T, Ibba I, Siju KP, Stensmyr MC, Hansson BS (2006) Olfactory shifts parallel superspecialism for toxic fruit in Drosophila melanogaster sibling, D. sechellia. Curr Biol 16:101–109

    CAS  PubMed  Google Scholar 

  • Denker M, Finke R, Schaupp F, Grün S, Menzel R (2010) Neural correlates of odor learning in the honeybee antennal lobe. Eur J Neurosci 31:119–133

    PubMed  Google Scholar 

  • Dinar N, Kaplan H, Kleiman M (1988) Characterization of concentration fluctuations of a surface plume in a neutral boundary layer. Bound-Layer Meteorol 45:157–175

    Google Scholar 

  • Dubnau J, Grady L, Kitamoto T, Tully T (2001) Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature 411:476–480

    CAS  PubMed  Google Scholar 

  • Durst C, Eichmüller S, Menzel R (1994) Development and experience lead to increased volume of subcompartments of the honeybee mushroom body. Behav Neural Biol 62:259–263

    CAS  PubMed  Google Scholar 

  • Elkinton JS, Schal C, Onot T, Cardé RT (1987) Pheromone puff trajectory and upwind flight of male gypsy moths in a forest. Physiol Entomol 12:399–406

    Google Scholar 

  • Ellen CW, Mercer AR (2012) Modulatory actions of dopamine and serotonin on insect antennal lobe neurons: insights from studies in vitro. J Mol Histol 43:401–404

    CAS  PubMed  Google Scholar 

  • El-Sayed AM (2014) The pherobase: database of pheromones and semiochemicals. http://www.pherobase.com/

  • Faber T, Joerges J, Menzel R (1999) Associative learning modifies neural representations of odors in the insect brain. Nat Neurosci 2:74–78

    CAS  PubMed  Google Scholar 

  • Farine J-P, Legal L, Moreteau B, Le Quere J-L (1996) Volatile components of ripe fruits of Morinda citrifolia and their effects on Drosophila. Phytochemistry 41:433–438

    CAS  Google Scholar 

  • Fernandez PC, Locatelli FF, Person-Rennell N, Deleo G, Smith BH (2009) Associative conditioning tunes transient dynamics of early olfactory processing. J Neurosci 29:10191–10202

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finelli CM, Pentcheff ND, Zimmer-Faust RK, Wethey DS (1999) Odor transport in turbulent flows: constraints on animal navigation. Limnol Oceanogr 44:1056–1071

    CAS  Google Scholar 

  • Finelli CM, Pentcheff ND, Zimmer RK, Wethey DS (2000) Physical constraints on ecological processes: a field test of odor-mediated foraging. Ecology 81:784–797

    Google Scholar 

  • Fişek M, Wilson RI (2013) Stereotyped connectivity and computations in higher-order olfactory neurons. Nat Neurosci 17:280–288

    PubMed  PubMed Central  Google Scholar 

  • Galizia CG (2014) Olfactory coding in the insect brain: data and conjectures. Eur J Neurosci 39:1784–1795

    PubMed  PubMed Central  Google Scholar 

  • Galizia CG, Rössler W (2010) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55:399–420

    CAS  PubMed  Google Scholar 

  • Galizia CG, Sachse S (2010) Odor coding in insects. In: Menini A (ed) The neurobiology of olfaction. CRC Press, Boca Raton, pp 35–70

    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

    CAS  PubMed  Google Scholar 

  • Goldsmith BR, Mitala JJ Jr, Josue J, Castro A, Lerner MB, Bayburt TH, Khamis SM, Jones RA, Brand JG, Sligar SG (2011) Biomimetic chemical sensors using nanoelectronic readout of olfactory receptor proteins. ACS Nanotechnol 5:5408–5416

    CAS  Google Scholar 

  • Gupta N, Stopfer M (2012) Functional analysis of a higher olfactory center, the lateral horn. J Neurosci 32:8138–8148

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63

    CAS  PubMed  Google Scholar 

  • Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711

    CAS  PubMed  Google Scholar 

  • Hansson BS, Ochieng SA, Grosmaitre X, Anton S, Njagi PGN (1996) Physiological responses and central nervous projections of antennal olfactory receptor neurons in the adult desert locust, Schistocerca gregaria (Orthoptera: Acrididae). J Comp Physiol A 179:157–167

    CAS  Google Scholar 

  • Harris GA, Nyadong L, Fernandez FM (2008) Recent developments in ambient ionization techniques for analytical mass spectrometry. Analyst 133:1297–1301

    CAS  PubMed  Google Scholar 

  • Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266–275

    CAS  PubMed  Google Scholar 

  • Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2:1–30

    CAS  PubMed  Google Scholar 

  • Hildebrand J (1995) Analysis of chemical signals by nervous systems. Proc Natl Acad Sci U S A 92:67–74

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595–631

    CAS  PubMed  Google Scholar 

  • Hildebrand JG, Christensen TA, Arbas EA, Hayashi JH, Homberg U, Kanzaki R, Stengl M (1992) Olfaction in Manduca sexta: cellular mechanisms of responses to sex pheromone. In: Duce IR (ed) Neurotox’91 – molecular basis of drug and pesticide action. Elsevier Applied Science, London, pp 323–338

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ibba I, Angioy A, Hansson B, Dekker T (2010) Macroglomeruli for fruit odors change blend preference in Drosophila. Naturwissenschaften 97:1059–1066

    CAS  PubMed  Google Scholar 

  • Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR Jr, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128:1187–1203

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaissling K (1986) Temporal characteristics of pheromone receptor cell responses in relation to orientation behaviour of moths. In: Payne TL, Birch MC, Kennedy CEJ (eds) Mechanisms in insect olfaction. Clarendon Press, Oxford, pp 193–199

    Google Scholar 

  • Kaissling KE, Thorson J (1980) Insect olfactory sensilla: structural, chemical and electrical aspects of the functional organization. In: Sattelle DB, Hall LM, Hildebrand JG (eds) Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier/North Holland Biomedical Press, Amsterdam, pp 261–282

    Google Scholar 

  • Kanzaki R, Arbas EA, Strausfeld NJ, Hildebrand JG (1989) Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. J Comp Physiol A 165:427–453

    CAS  PubMed  Google Scholar 

  • Kanzaki R, Arbas E, Hildebrand J (1991) Physiology and morphology of descending neurons in pheromone-processing olfactory pathways in the male moth Manduca sexta. J Comp Physiol A 169:1–14

    CAS  PubMed  Google Scholar 

  • Kanzaki R, Ikeda A, Shibuya T (1994) Morphological and physiological-properties of pheromone-triggered flipflop** descending interneurons of the male silkworm moth, Bombyx mori. J Comp Physiol A 175:1–14

    CAS  Google Scholar 

  • Kanzaki R, Soo K, Seki Y, Wada S (2003) Projections to higher olfactory centers from subdivisions of the antennal lobe macroglomerular complex of the male silkmoth. Chem Senses 28:113–130

    CAS  PubMed  Google Scholar 

  • Kárpáti Z, Knaden M, Reinecke A, Hansson BS (2013) Intraspecific combinations of flower and leaf volatiles act together in attracting hawkmoth pollinators. PLoS One 8:e72805

    PubMed  PubMed Central  Google Scholar 

  • Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grünewald B, Rössler W (2006) Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499:933–952

    PubMed  Google Scholar 

  • Kloppenburg P, Mercer AR (2008) Serotonin modulation of moth central olfactory neurons. Annu Rev Entomol 53:179–190

    CAS  PubMed  Google Scholar 

  • Koehl MAR (2006) The fluid mechanics of arthropod sniffing in turbulent odor plumes. Chem Senses 31:93–105

    CAS  PubMed  Google Scholar 

  • Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3:884–895

    CAS  PubMed  Google Scholar 

  • Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373–391

    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

    CAS  PubMed  Google Scholar 

  • Lei H, Christensen TA, Hildebrand JG (2004) Spatial and temporal organization of ensemble representations for different odor classes in the moth antennal lobe. J Neurosci 24:11108–11119

    CAS  PubMed  Google Scholar 

  • Lei H, Riffell J, Gage S, Hildebrand J (2009) Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance. J Biol 8:21

    PubMed  PubMed Central  Google Scholar 

  • Lei H, Chiu H-Y, Hildebrand JG (2013) Responses of protocerebral neurons in Manduca sexta to sex-pheromone mixtures. J Comp Physiol A 199:997–1014

    CAS  Google Scholar 

  • Lemon W, Getz W (1997) Temporal resolution of general odor pulses by olfactory sensory neurons in American cockroaches. J Exp Biol 200:1809–1819

    CAS  PubMed  Google Scholar 

  • Lemon WC, Getz WM (2000) Rate code input produces temporal code output from cockroach antennal lobes. Biosystems 58:151–158

    CAS  PubMed  Google Scholar 

  • Liang L, Li Y, Potter CJ, Yizhar O, Deisseroth K, Tsien RW, Luo L (2013) GABAergic projection neurons route selective olfactory inputs to specific higher-order neurons. Neuron 79:917–931

    CAS  PubMed  Google Scholar 

  • Linster C, Sachse S, Galizia CG (2005) Computational modeling suggests that response properties rather than spatial position determine connectivity between olfactory glomeruli. J Neurophysiol 93:3410–3417

    PubMed  Google Scholar 

  • Loudon C, Koehl MAR (2000) Sniffing by a silkworm moth: wing fanning enhances air penetration through and pheromone interception by antennae. J Exp Biol 203:2977–2990

    CAS  PubMed  Google Scholar 

  • Loudon C, Best BA, Koehl MAR (1994) When does motion relative to neighboring surfaces alter the flow-through arrays of hairs. J Exp Biol 193:233–254

    CAS  PubMed  Google Scholar 

  • Mafra-Neto A, Carde RT (1994) Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths. Nature 369:142–144

    CAS  Google Scholar 

  • Marion-Poll F, Tobin T (1992) Temporal coding of pheromone pulses and trains in Manduca sexta. J Comp Physiol A 171:505–512

    CAS  PubMed  Google Scholar 

  • Martin JP, Beyerlein A, Dacks AM, Reisenman CE, Riffell JA, Lei H, Hildebrand JG (2011) The neurobiology of insect olfaction: sensory processing in a comparative context. Prog Neurobiol 95:427–447

    PubMed  Google Scholar 

  • Martin JP, Lei H, Riffell JA, Hildebrand JG (2013) Synchronous firing of antennal-lobe projection neurons encodes the behaviorally effective ratio of sex-pheromone components in male Manduca sexta. J Comp Physiol A 199:963–979

    CAS  Google Scholar 

  • Matsumoto SG, Hildebrand JG (1981) Olfactory mechanisms in the moth Manduca sexta: response characteristics and morphology of central neurons in the antennal lobes. Proc R Soc Lond B 213:249–277

    CAS  Google Scholar 

  • Mole N, Jones C (1994) Concentration fluctuation data from dispersion experiments carried out in stable and unstable conditions. Bound-Layer Meteorol 67:41–74

    Google Scholar 

  • Moore P, Crimaldi J (2004) Odor landscapes and animal behavior: tracking odor plumes in different physical worlds. J Mar Syst 49:55–64

    Google Scholar 

  • Moorhouse JE, Yeadon R, Beevor PS, Nesbitt BF (1969) Method for use in studies of insect chemical communication. Nature 223:1174–1175

    CAS  Google Scholar 

  • Murlis J, Elkinton JS, Carde RT (1992) Odor plumes and how insects use them. Annu Rev Entomol 37:505–532

    Google Scholar 

  • Mwilaria EK, Ghatak C, Daly KC (2008) Disruption of GABA A in the insect antennal lobe generally increases odor detection and discrimination thresholds. Chem Senses 33:267–281

    CAS  PubMed  Google Scholar 

  • Mylne KR, Mason P (1991) Concentration fluctuation measurements in a dispersing plume at a range of up to 1000 m. Q J R Meteorol Soc 117:177–206

    Google Scholar 

  • Ochieng S, Park K, Baker T (2002) Host plant volatiles synergize responses of sex pheromone-specific olfactory receptor neurons in male Helicoverpa zea. J Comp Physiol A 188:325–333

    CAS  Google Scholar 

  • Okada R, Sakura M, Mizunami M (2003) Distribution of dendrites of descending neurons and its implications for the basic organization of the cockroach brain. J Comp Neurol 458:158–174

    PubMed  Google Scholar 

  • Olsen SR, Wilson RI (2008) Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452:956–960

    CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen SR, Bhandawat V, Wilson RI (2007) Excitatory Interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54:89–103

    CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen SR, Bhandawat V, Wilson RI (2010) Divisive normalization in olfactory population codes. Neuron 66:287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parnas M, Lin AC, Huetteroth W, Miesenböck G (2013) Odor discrimination in Drosophila: from neural population codes to behavior. Neuron 79:932–944

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peakall R (1990) Responses of male Zaspilothynnus trilobatus turner wasps to females and the sexually deceptive orchid it pollinates. Funct Ecol 159–167

    Google Scholar 

  • Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, Laurent G (2002) Oscillations and sparsening of odor representations in the mushroom body. Science 297:359–365

    CAS  PubMed  Google Scholar 

  • Pregitzer P, Schubert M, Breer H, Hansson BS, Sachse S, Krieger J (2012) Plant odorants interfere with detection of sex pheromone signals by male Heliothis virescens. Front Cell Neurosci 6:42

    PubMed  PubMed Central  Google Scholar 

  • Raguso RA, Henzel C, Buchman SL, Nabhan GP (2003) Trumpet flowers of the Sonoran Desert: floral biology of Peniocereus cacti and Sacred Datura. Int J Plant Sci 164:877–892

    CAS  Google Scholar 

  • Reinhard J, Srinivasan MV, Guez D, Zhang SW (2004) Floral scents induce recall of navigational and visual memories in honeybees. J Exp Biol 207:4371–4381

    PubMed  Google Scholar 

  • Reinhard J, Sinclair M, Srinivasan MV, Claudianos C (2010) Honeybees learn odour mixtures via a selection of key odorants. PLoS ONE 5:e9110

    PubMed  PubMed Central  Google Scholar 

  • Riffell JA, Abrell L, Hildebrand JG (2008) Physical processes and real-time chemical measurement of the insect olfactory environment. J Chem Ecol 34:837–853

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riffell JA, Lei H, Christensen TA, Hildebrand JG (2009a) Characterization and coding of behaviorally significant odor mixtures. Curr Biol 19:335–340

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riffell JA, Lei H, Hildebrand JG (2009b) Neural correlates of behavior in the moth Manduca sexta in response to complex odors. Proc Natl Acad Sci U S A 106:19219–19226

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riffell JA, Lei H, Abrell L, Hildebrand JG (2013) Neural basis of a pollinator’s buffet: olfactory specialization and learning in Manduca sexta. Science 339:200–204

    CAS  PubMed  Google Scholar 

  • Riffell JA, Shlizerman E, Sanders E, Abrell L, Medina B, Hinterwirth AJ, Kutz JN (2014) Flower discrimination by pollinators in a dynamic chemical environment. Science 344:1515–1518

    CAS  PubMed  Google Scholar 

  • Rø H, Müller D, Mustaparta H (2007) Anatomical organization of antennal lobe projection neurons in the moth Heliothis virescens. J Comp Neurol 500:658–675

    PubMed  Google Scholar 

  • Roelofs WL, Comeau A, Hill A, Milicevic G (1971) Sex attractant of the codling moth: characterization with electroantennogram technique. Science 174:297–299

    CAS  PubMed  Google Scholar 

  • Root CM, Semmelhack JL, Wong AM, Flores J, Wang JW (2007) Propagation of olfactory information in Drosophila. Proc Natl Acad Sci U S A 104:11826–11831

    CAS  PubMed  PubMed Central  Google Scholar 

  • Root CM, Ko KI, Jafari A, Wang JW (2011) Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145:133–144

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roussel E, Carcaud J, Combe M, Giurfa M, Sandoz J-C (2014) Olfactory coding in the honeybee lateral horn. Curr Biol 24:561–567

    CAS  PubMed  Google Scholar 

  • Rumbo E, Kaissling K-E (1989) Temporal resolution of odour pulses by three types of pheromone receptor cells in Antheraea polyphemus. J Comp Physiol A 165:281–291

    Google Scholar 

  • Rybak J, Menzel R (1993) Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha‐lobe. J Comp Neurol 334:444–465

    CAS  PubMed  Google Scholar 

  • Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106–1117

    PubMed  Google Scholar 

  • Sane SP (2006) Induced airflow in flying insects I. A theoretical model of the induced flow. J Exp Biol 209:32–42

    PubMed  Google Scholar 

  • Sane SP, Jacobson NP (2006) Induced airflow in flying insects II. Measurement of induced flow. J Exp Biol 209:43–56

    PubMed  Google Scholar 

  • Schiestl FP, Ayasse M, Paulus HF, Löfstedt C, Hansson BS, Ibarra F, Francke W (1999) Orchid pollination by sexual swindle. Nature 399:421–421

    Google Scholar 

  • Schiestl FP, Peakall R, Mant JG, Ibarra F, Schulz C, Franke S, Francke W (2003) The chemistry of sexual deception in an orchid-wasp pollination system. Science 302:437–438

    CAS  PubMed  Google Scholar 

  • Schneider D (1957) Elektrophysiologische Untersuchungen von Chemo- und Mechanorezeptoren der Antenne des Seidenspinners Bombyx mori L. J Comp Physiol A 40:8–41

    Google Scholar 

  • Schröder R, Hilker M (2008) The relevance of background odor in resource location by insects: a behavioral approach. Bioscience 58:308–316

    Google Scholar 

  • Schubert M, Hansson BS, Sachse S (2014) The banana code—natural blend processing in the olfactory circuitry of Drosophila melanogaster. Front Physiol 5:59

    PubMed  PubMed Central  Google Scholar 

  • Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495–10502

    CAS  PubMed  Google Scholar 

  • Seki Y, Aonuma H, Kanzaki R (2005) Pheromone processing center in the protocerebrum of Bombyx mori revealed by nitric oxide‐induced anti‐cGMP immunocytochemistry. J Comp Neurol 481:340–351

    CAS  PubMed  Google Scholar 

  • Shimizu K, Stopfer M (2012) Olfaction: intimate neuronal whispers. Nature 492:44–45

    CAS  PubMed  Google Scholar 

  • Silbering AF, Galizia CG (2007) Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966–11977

    CAS  PubMed  Google Scholar 

  • Sprayberry JD, Daniel TL (2007) Flower tracking in hawkmoths: behavior and energetics. J Exp Biol 210:37–45

    PubMed  Google Scholar 

  • Stocker RF, Lienhard MC, Borst A, Fischbach K-F (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9–34

    CAS  PubMed  Google Scholar 

  • Stockhouse REI (1976) A new method for studying pollen dispersal using micronized fluorescent dusts. Am Midl Nat 96:241–245

    Google Scholar 

  • Strausfeld NJ (2012) Arthropod brains: evolution, functional elegance, and historical significance. Belknap Press of Harvard University Press, Cambridge, MA

    Google Scholar 

  • Strausfeld NJ, Bushbeck EK, Gomez RS (1995) The arthropod mushroom body: its functional roles, evolutionary enigmas and mistaken identities. In: Breidback O, Kutsch W (eds) The nervous system of invertebrates, a evolutionary and comparative approach. Birkhäuser, Basel, pp 349–381

    Google Scholar 

  • Strube-Bloss MF, Nawrot MP, Menzel R (2011) Mushroom body output neurons encode odor–reward associations. J Neurosci 31:3129–3140

    CAS  PubMed  Google Scholar 

  • Strube-Bloss MF, Herrera-Valdez MA, Smith BH (2012) Ensemble response in mushroom body output neurons of the honey bee outpaces spatiotemporal odor processing two synapses earlier in the antennal lobe. PLoS One 7:e50322

    CAS  PubMed  PubMed Central  Google Scholar 

  • Su C-Y, Martelli C, Emonet T, Carlson JR (2011) Temporal coding of odor mixtures in an olfactory receptor neuron. Proc Natl Acad Sci U S A 108:5075–5080

    CAS  PubMed  PubMed Central  Google Scholar 

  • Su C-Y, Menuz K, Reisert J, Carlson JR (2012) Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 492:66–71

    CAS  PubMed  PubMed Central  Google Scholar 

  • Szyszka P, Ditzen M, Galkin A, Galizia CG, Menzel R (2005) Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J Neurophysiol 94:3303–3313

    PubMed  Google Scholar 

  • Szyszka P, Galkin A, Menzel R (2008) Associative and non-associative plasticity in Kenyon cells of the honeybee mushroom body. Front Syst Neurosci 2:3

    PubMed  PubMed Central  Google Scholar 

  • Tholl D, Röse USR (2006) Detection and identification of floral scent compounds. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Taylor Francis, Boca Raton, pp 3–25

    Google Scholar 

  • Tomchik SM, Davis RL (2009) Dynamics of learning-related cAMP signaling and stimulus integration in the Drosophila olfactory pathway. Neuron 64:510–521

    CAS  PubMed  PubMed Central  Google Scholar 

  • Turner GC, Bazhenov M, Laurent G (2008) Olfactory representations by Drosophila mushroom body neurons. J Neurophysiol 99:734–746

    PubMed  Google Scholar 

  • Van Breugel F, Dickinson MH (2014) Plume-tracking behavior of flying Drosophila emerges from a set of distinct sensory-motor reflexes. Curr Biol 24:274–286

    PubMed  Google Scholar 

  • Van Der Pers J, Thomas G, Den Otter C (1980) Interactions between plant odours and pheromone reception in small ermine moths (Lepidoptera: Yponomeutidae). Chem Senses 5:367–371

    Google Scholar 

  • Vickers N, Baker T (1994) Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. Proc Natl Acad Sci U S A 91:5756–5760

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weissburg M (2000) The fluid dynamical context of chemosensory behavior. Biol Bull 198:188–202

    CAS  PubMed  Google Scholar 

  • Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366–370

    CAS  PubMed  Google Scholar 

  • Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229–241

    CAS  PubMed  Google Scholar 

  • Wright GA, Smith BH (2004) Variation in complex olfactory stimuli and its influence on odour recognition. Proc R Soc Lond Ser B 271:147–152

    Google Scholar 

  • Yaksi E, Wilson RI (2010) Electrical coupling between olfactory glomeruli. Neuron 67:1034–1047

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yee E, Kosteniuk P, Chandler G, Biltoft C, Bowers J (1993a) Statistical characteristics of concentration fluctuations in dispersing plumes in the atmospheric surface layer. Bound-Layer Meteorol 65:69–109

    Google Scholar 

  • Yee E, Wilson D, Zelt B (1993b) Probability distributions of concentration fluctuations of a weakly diffusive passive plume in a turbulent boundary layer. Bound-Layer Meteorol 64:321–354

    Google Scholar 

  • Yu D, Ponomarev A, Davis RL (2004) Altered representation of the spatial code for odors after olfactory classical conditioning: memory trace formation by synaptic recruitment. Neuron 42:437–449

    CAS  PubMed  Google Scholar 

  • Zimmer RK, Zimmer C (2008) Dynamic scaling in chemical ecology. J Chem Ecol 34:822–836

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank E. Warrant and G. von der Emde for their invitation to be included in this book. We also thank H. Lei, C. Reisenman, E. Shlizerman, and M. Dickinson for discussions on olfactory filtering and processing. Funding was provided by National Science Foundation (IOS-1354159 and DMS-1361145), the National Institutes of Health (R01DC013693, R01DC02751), and the Human Frontier Science Program (A87616).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeffrey A. Riffell .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Riffell, J.A., Hildebrand, J.G. (2016). Adaptive Processing in the Insect Olfactory System. In: von der Emde, G., Warrant, E. (eds) The Ecology of Animal Senses. Springer, Cham. https://doi.org/10.1007/978-3-319-25492-0_1

Download citation

Publish with us

Policies and ethics

Navigation