Skip to main content
SpringerLink
Log in

Synchronous firing of antennal-lobe projection neurons encodes the behaviorally effective ratio of sex-pheromone components in male Manduca sexta

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Olfactory stimuli that are essential to an animal’s survival and reproduction are often complex mixtures of volatile organic compounds in characteristic proportions. Here, we investigated how these proportions are encoded in the primary olfactory processing center, the antennal lobe, of male Manduca sexta moths. Two key components of the female’s sex pheromone, present in an approximately 2:1 ratio, are processed in each of two neighboring glomeruli in the macroglomerular complex (MGC) of males of this species. In wind-tunnel flight experiments, males exhibited behavioral selectivity for ratios approximating the ratio released by conspecific females. The ratio between components was poorly represented, however, in the firing-rate output of uniglomerular MGC projection neurons (PNs). PN firing rate was mostly insensitive to the ratio between components, and individual PNs did not exhibit a preference for a particular ratio. Recording simultaneously from pairs of PNs in the same glomerulus, we found that the natural ratio between components elicited the most synchronous spikes, and altering the proportion of either component decreased the proportion of synchronous spikes. The degree of synchronous firing between PNs in the same glomerulus thus selectively encodes the natural ratio that most effectively evokes the natural behavioral response to pheromone.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AL:

Antennal lobe

BAL:

Bombykal, (E,Z)-10,12-hexadecadienal

EAG:

Electroantennogram

EEZ:

(E,E,Z)-10,12-14-hexadecatrienal

MGC:

Macroglomerular complex

mPN:

Multi-glomerular projection neuron

ORC:

Olfactory receptor cell

PN:

Projection neuron

uPN:

Uniglomerular projection neuron

VOC:

Volatile organic compound

References

  • Alonso JM, Usrey WM, Reid RC (1996) Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383:815–819

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Atick JJ (1992) Could information theory provide an ecological theory of sensory processing? Netw Comput Neural Syst 3:213–251

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Baker TC, Cardé RT (1979) Analysis of pheromone-mediated behaviors in male Grapholitha molesta, the oriental fruit moth (Lepidoptera: Tortricidae). Environ Entomol 8:956–968

    CAS  Google Scholar 

  • Baker TC, Meyer W, Roelofs WL (1981) Sex pheromone dosage and blend specificity of response by oriental fruit moth males. Entomol Exp Appl 30:269–279

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Biederlack J, Castelo-Branco M, Neuenschwander S, Wheeler DW, Singer W, Nikolic D (2006) Brightness induction: rate enhancement and neuronal synchronization as complementary codes. Neuron 52:1073–1083

    Article  PubMed  CAS  Google Scholar 

  • Boeckh J, Boeckh V (1979) Threshold and odor specificity of pheromone-sensitive neurons in the deutocerebrum of Antheraea pernyi and Antheraea polyphemus (Saturnidae). J Comp Physiol A 132:235–242

    Article  CAS  Google Scholar 

  • Brandstaetter AS, Roessler W, Kleineidam CJ (2011) Friends and foes from an ant brain’s point of view—neuronal correlates of colony odors in a social insect. PLoS One 6(6):e21383

    Article  PubMed  CAS  Google Scholar 

  • Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274

    Article  PubMed  CAS  Google Scholar 

  • Budick SA, Reiser MB, Dickinson MH (2007) The role of visual and mechanosensory cues in structuring forward flight in Drosophila melanogaster. J Exp Biol 210:4092–4103

    Article  PubMed  Google Scholar 

  • Cardé RT, Minks AK (1995) Control of moth pests by mating disruption—successes and constraints. Annu Rev Entomol 40:559–585

    Article  Google Scholar 

  • Carlsson MA, Chong KY, Daniels W, Hansson BS, Pearce TC (2007) Component information is preserved in glomerular responses to binary odor mixtures in the moth Spodoptera littoralis. Chem Senses 32:433–443

    Article  PubMed  CAS  Google Scholar 

  • Cha DH, Linn CE, Teal PEA, Zhang AJ, Roelofs WL, Loeb GM (2011) Eavesdropping on plant volatiles by a specialist moth: significance of ratio and concentration. PLoS One 6:8

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Christensen TA, Hildebrand JG (1987b) Pheromonal information coding by projection neurons in the antennal lobes of the sphinx moth Manduca sexta. Ann N Y Acad Sci 510:224–226

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Christensen TA, Itagaki H, Teal PEA, Jasensky RD, Tumlinson JH, Hildebrand JG (1991) Innervation and neural regulation of the sex-pheromone gland in female Heliothis moths. Proc Natl Acad Sci USA 88:4971–4975

    Article  PubMed  CAS  Google Scholar 

  • Christensen TA, Mustaparta H, Hildebrand JG (1995) Chemical communication in heliothine moths 6. Parallel pathways for information-processing in the macroglomerular complex of the male tobacco budworm moth Heliothis virescens. J Comp Physiol A 177:545–557

    Article  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

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Christensen TA, Lei H, Hildebrand JG (2003) Coordination of central odor representations through transient non-oscillatory synchronization of glomerular output neurons. Proc Natl Acad Sci USA 100:11076–11081

    Article  PubMed  CAS  Google Scholar 

  • Clifford MR, Riffell JA (2013) Mixture and odorant processing in the olfactory systems of insects: a comparative perspective. J Comp Physiol A. doi:10.1007/s00359-013-0818-6

    Google Scholar 

  • Dan Y, Alonso JM, Usrey WM, Reid RC (1998) Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus. Nat Neurosci 1:501–507

    Article  PubMed  CAS  Google Scholar 

  • deCharms RC, Merzenich MM (1996) Primary cortical representation of sounds by the coordination of action-potential timing. Nature 381:610–613

    Article  PubMed  CAS  Google Scholar 

  • Deisig N, Giurfa M, Lachnit H, Sandoz J-C (2006) Neural representation of olfactory mixtures in the honeybee antennal lobe. Eur J Neurosci 24:1161–1174

    Article  PubMed  Google Scholar 

  • Dunkelblum E, Mazor M (1993) Chemical characterization and species specificity of sex-pheromones of plusiinae moths in Israel. Arch Insect Biochem Physiol 22:413–424

    Article  CAS  Google Scholar 

  • Dusenberry DB (1992) Sensory ecology: How animals acquire and respond to information?. Freeman, New York

    Google Scholar 

  • El-Sayed A, Bengtsson M, Rauscher S, Lofqvist J, Witzgall P (1999) Multicomponent sex pheromone in codling moth (Lepidoptera: Tortricidae). Environ Entomol 28:775–779

    CAS  Google Scholar 

  • Ewert JP (1997) Neural correlates of key stimulus and releasing mechanism: a case study and two concepts. Trends Neurosci 20:332–339

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Friedrich RW, Habermann CJ, Laurent G (2004) Multiplexing using synchrony in the zebrafish olfactory bulb. Nat Neurosci 7:862–871

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Galizia CG, Szyszka P (2008) Olfactory coding in the insect brain: molecular receptive ranges, spatial and temporal coding. Entomol Exp Appl 128:81–92

    Article  Google Scholar 

  • Garcia-Lazaro JA, Ahmed B, Schnupp JWH (2006) Tuning to natural stimulus dynamics in primary auditory cortex. Curr Biol 16:264–271

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hansson BS, Anton S, Christensen TA (1994) Structure and function of antennal lobe neurons in the male turnip moth, Agrotis segetum (Lepidoptera: Noctuidae). J Comp Physiol A 175:547–562

    Article  Google Scholar 

  • Hartlieb E, Anton S, Hansson BS (1997) Dose-dependent response characteristics of antennal lobe neurons in the male moth Agrotis segetum (Lepidoptera: Noctuidae). J Comp Physiol A 181:469–476

    Article  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  PubMed  CAS  Google Scholar 

  • Heinbockel T, Christensen TA, Hildebrand JG (2004) Representation of binary pheromone blends by glomerulus-specific olfactory projection neurons. J Comp Physiol A 190:1023–1037

    Article  CAS  Google Scholar 

  • Homberg U, Montague RA, Hildebrand JG (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254:255–281

    Article  PubMed  CAS  Google Scholar 

  • Jarriault D, Gadenne C, Rospars JP, Anton S (2009) Quantitative analysis of sex-pheromone coding in the antennal lobe of the moth Agrotis ipsilon: a tool to study network plasticity. J Exp Biol 212:1191–1201

    Article  PubMed  Google Scholar 

  • Jinks A, Laing DG (2001) The analysis of odor mixtures by humans: evidence for a configurational process. Physiol Behav 72:51–63

    Article  PubMed  CAS  Google Scholar 

  • Johnson BA, Ong J, Leon M (2010) Glomerular activity patterns evoked by natural odor objects in the rat olfactory bulb are related to 14 patterns evoked by major odorant components. J Comp Neurol 518:1542–1555

    Article  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

    Article  CAS  Google Scholar 

  • Kalinova B, Hoskovec M, Liblikas I, Unelius CR, Hansson BS (2001) Detection of sex pheromone components in Manduca sexta (L.). Chem Senses 26:1175–1186

    Article  PubMed  CAS  Google Scholar 

  • Kanzaki R, Shibuya T (1983) Olfactory neural pathway and sexual pheromone responses in the deutocerebrum of the male silkworm moth, Bombyx mori (Lepidoptera: Bombycidae). Appl Ent Zool 18:131–133

    CAS  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

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Kashiwadani H, Sasaki YF, Uchida N, Mori K (1999) Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J Neurophysiol 82:1786–1792

    PubMed  CAS  Google Scholar 

  • Kazama H, Wilson RI (2009) Origins of correlated activity in an olfactory circuit. Nat Neurosci 12:1136–1144

    Article  PubMed  CAS  Google Scholar 

  • Khan AG, Thattai M, Bhalla US (2008) Odor representations in the rat olfactory bulb change smoothly with morphing stimuli. Neuron 57:571–585

    Article  PubMed  CAS  Google Scholar 

  • Kohn A, Smith MA (2005) Stimulus dependence of neuronal correlation in primary visual cortex of the macaque. J Neurosci 25:3661–3673

    Article  PubMed  CAS  Google Scholar 

  • Koulakov A, Gelperin A, Rinberg D (2007) Olfactory coding with all-or-nothing glomeruli. J Neurophysiol 98:3134–3142

    Article  PubMed  Google Scholar 

  • Kruskal PB, Stanis JJ, McNaughton BL, Thomas PJ (2007) A binless correlation measure reduces the variability of memory reactivation estimates. Stat Med 26:3997–4008

    Article  PubMed  Google Scholar 

  • Kuebler LS, Olsson SB, Weniger R, Hansson BS (2011) Neuronal processing of complex mixtures establishes a unique odor representation in the moth antennal lobe. Front Neural Circuits 5:7

    Article  PubMed  Google Scholar 

  • Lei H, Vickers N (2008) Central processing of natural odor mixtures in insects. J Chem Ecol 34:915–927

    Article  PubMed  CAS  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  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lei H, Reisenman CE, Wilson CH, Gabbur P, Hildebrand JG (2011) Spiking patterns and their functional implications in the antennal lobe of the tobacco hornworm Manduca sexta. PLoS One 6:e23382

    Article  PubMed  CAS  Google Scholar 

  • Lei H, Chu H-Y, Hildebrand JG (2013) Responses of protocerebral neurons in Manduca sexta to sex-pheromone mixtures. J Comp Physiol A. doi:10.1007/s00359-013-0844-4

    Google Scholar 

  • Leon M, Johnson B (2006) Functional units in the olfactory system. Proc Natl Acad Sci USA 103:14985–14986

    Article  PubMed  CAS  Google Scholar 

  • Linn CE, Roelofs WL (1983) Effect of varying proportions of the alcohol component on sex pheromone blend discrimination in male oriental fruit moths. Physiol Entomol 8:291–306

    Article  CAS  Google Scholar 

  • Linn CE, Roelofs WL (1985) Response specificity of male pink-bollworm moths to different blends and dosages of sex-pheromone. J Chem Ecol 11:1583–1590

    Article  CAS  Google Scholar 

  • Linn CE, Campbell MG, Roelofs WL (1988) Temperature modulation of behavioral thresholds controlling male moth sex-pheromone response specificity. Physiol Entomol 13:59–67

    Article  CAS  Google Scholar 

  • Linn C, Campbell M, Roelofs W (1991) The effects of different blend ratios and temperature on the active space of the oriental fruit moth sex-pheromone. Physiol Entomol 16:211–222

    Article  CAS  Google Scholar 

  • Löfstedt C, Pers JN (1985) Sex pheromones and reproductive isolation in four European small ermine moths. J Chem Ecol 11:649–666

    Article  Google Scholar 

  • Löfstedt C, Herrebout WM, Menken SBJ (1991) Sex pheromones and their potential role in the evolution of reproductive isolation in small ermine moths (Yponomeutidae). Chemoecol 2:20–28

    Article  Google Scholar 

  • Lyttle D, Fellous JM (2011) A new similarity measure for spike trains: sensitivity to bursts and periods of inhibition. J Neurosci Meth 199:296–309

    Article  Google Scholar 

  • Machens CK, Stemmler MB, Prinz P, Krahe R, Ronacher B, Herz AVM (2001) Representation of acoustic communication signals by insect auditory receptor neurons. J Neurosci 21:3215–3227

    PubMed  CAS  Google Scholar 

  • Magee JC (2000) Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1:181–190

    Article  PubMed  CAS  Google Scholar 

  • Martin JP, Hildebrand JG (2010) Innate recognition of pheromone and food odors in moths: a common mechanism in the antennal lobe? Front Behav Neurosci 4:159

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Mastronarde DN (1983) Interactions between Ganglion-cells in cat retina. J Neurophysiol 49:350–365

    PubMed  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 B 213:249–277

    Article  CAS  Google Scholar 

  • Meister M (1996) Multineuronal codes in retinal signaling. Proc Natl Acad Sci USA 93:609–614

    Article  PubMed  CAS  Google Scholar 

  • Ming QL, Yan YH, Wang CZ (2007) Mechanisms of premating isolation between Helicoverpa armigera (Hubner) and Helicoverpa assulta (Guenee) (Lepidoptera : Noctuidae). J Insect Physiol 53:170–178

    Article  PubMed  CAS  Google Scholar 

  • Minks AK, Cardé RT (1988) Disruption of pheromone communication in moths—is the natural blend really most efficacious? Entomol Exp Appl 49:25–36

    Article  Google Scholar 

  • Minks AK, Roelofs WL, Ritter FJ, Persoons CJ (1973) Reproductive isolation of 2 tortricid moth species by different ratios of a 2 component sex attractant. Science 180:1073–1074

    Article  PubMed  CAS  Google Scholar 

  • Najar-Rodriguez AJ, Galizia CG, Stierle J, Dorn S (2010) Behavioral and neurophysiological responses of an insect to changing ratios of constituents in host plant-derived volatile mixtures. J Exp Biol 213(19):3388–3397

    Article  PubMed  CAS  Google Scholar 

  • Nowak LG, Munk MHJ, Nelson JI, James AC, Bullier J (1995) Structural basis of cortical synchronization 1. Three types of interhemispheric coupling. J Neurophysiol 74:2379–2400

    PubMed  CAS  Google Scholar 

  • Olsen SR, Bhandawat V, Wilson RI (2010) Divisive normalization in olfactory population codes. Neuron 66:287–299

    Article  PubMed  CAS  Google Scholar 

  • Paiva ARC, Park I, Principe JC (2010) A comparison of binless spike train measures. Neural Comput Appl 19:405–419

    Article  Google Scholar 

  • Panzeri S, Brunel N, Logothetis NK, Kayser C (2010) Sensory neural codes using multiplexed temporal scales. Trends Neurosci 33:111–120

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Perez-Orive J, Bazhenov M, Laurent G (2004) Intrinsic and circuit properties favor coincidence detection for decoding oscillatory input. J Neurosci 24:6037–6047

    Article  PubMed  CAS  Google Scholar 

  • Perkel DH, Gerstein GL, Moore GP (1967a) Neuronal spike trains and stochastic point processes I. The single spike train. Biophys J 7:391–418

    Article  PubMed  CAS  Google Scholar 

  • Perkel DH, Gerstein GL, Moore GP (1967b) Neuronal spike trains and stochastic point processes II. Simultaneous spike trains. Biophys J 7:419–440

    Article  PubMed  CAS  Google Scholar 

  • Pinault D (1996) A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly-labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J Neurosci Meth 65:113–136

    Article  CAS  Google Scholar 

  • Puopolo M, Belluzzi O (2001) NMDA-dependent, network-driven oscillatory activity induced by bicuculline or removal of Mg2+ in rat olfactory bulb neurons. Eur J Neurosci 13:92–102

    Article  PubMed  CAS  Google Scholar 

  • Quero C, Baker TC (1999) Antagonistic effect of (Z)-11-hexadecen-1-ol on the pheromone-mediated flight of Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae). J Insect Behav 12:701–710

    Article  Google Scholar 

  • Riehle A, Grun S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278:1950–1953

    Article  PubMed  CAS  Google Scholar 

  • Rieke F, Bodnar DA, Bialek W (1995) Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents. Proc R Soc Lond B 262(1365):259–265

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 USA 106:19219–19226

    Article  PubMed  CAS  Google Scholar 

  • Roelofs WL (1978) Threshold hypothesis for pheromone perception. J Chem Ecol 4:685–699

    Article  CAS  Google Scholar 

  • Roelofs WL, Cardé RT (1977) Responses of Lepidoptera to synthetic sex-pheromone chemicals and their analogs. Annu Rev Entomol 22:377–405

    Article  CAS  Google Scholar 

  • Rolls ET, Tovee MJ, Purcell DG, Stewart AL, Azzopardi P (1994) The responses of neurons in the temporal cortex of primates, and face identification and detection. Exp Brain Res 101:473–484

    Article  PubMed  CAS  Google Scholar 

  • Sane SP, Dieudonné A, Willis MA, Daniel TL (2007) Antennal mechanosensors mediate flight control in moths. Science 315:863–866

    Google Scholar 

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

    Article  Google Scholar 

  • Schlyter F, Svensson M, Zhang QH, Knizek M, Krokene P, Ivarsson P, Birgersson G (2001) A model for peak and width of signaling windows: Ips duplicatus and Chilo partellus pheromone component proportions—does response have a wider window than production? J Chem Ecol 27:1481–1511

    Article  PubMed  CAS  Google Scholar 

  • Schnitzer MJ, Meister M (2003) Multineuronal firing patterns in the signal from eye to brain. Neuron 37:499–511

    Article  PubMed  CAS  Google Scholar 

  • Schoppa NE (2006a) AMPA/kainate receptors drive rapid output and precise synchrony in olfactory bulb granule cells. J Neurosci 26:12996–13006

    Article  PubMed  CAS  Google Scholar 

  • Schoppa NE (2006b) Synchronization of olfactory bulb mitral cells by precisely timed inhibitory inputs. Neuron 49:271–283

    Article  PubMed  CAS  Google Scholar 

  • Schoppa NE, Westbrook GL (2001) Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 31:639–651

    Article  PubMed  CAS  Google Scholar 

  • Schreiber S, Fellous JM, Whitmer D, Tiesinga P, Sejnowski TJ (2003) A new correlation-based measure of spike timing reliability. Neurocomputing 54:925–931

    Article  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Silbering AF, Okada R, Ito K, Galizia CG (2008) Olfactory information processing in the Drosophila antennal lobe: anything goes? J Neurosci 28:13075–13087

    Article  PubMed  CAS  Google Scholar 

  • Silva IM, Eiras AE, Kline DL, Bernier UR (2005) Laboratory evaluation of mosquito traps baited with a synthetic human odor blend to capture Aedes aegypti. J Am Mosquito Control Assoc 21:229–233

    Article  Google Scholar 

  • Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations. Neuron 24:49–65

    Article  PubMed  CAS  Google Scholar 

  • Softky WR, Koch C (1993) The highly irregular firing of cortical-cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334–350

    PubMed  CAS  Google Scholar 

  • Swadlow HA, Beloozerova IN, Sirota MG (1998) Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. J Neurophysiol 79:567–582

    PubMed  CAS  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

    Article  PubMed  Google Scholar 

  • Tabor R, Yaksi E, Weislogel JM, Friedrich RW (2004) Processing of odor mixtures in the zebrafish olfactory bulb. J Neurosci 24:6611–6620

    Article  PubMed  CAS  Google Scholar 

  • Takahashi S, Sakurai Y (2009) Sub-millisecond firing synchrony of closely neighboring pyramidal neurons in hippocampal CA1 of rats during delayed non-matching to sample task. Front Neural Circuits 3:9

    Article  PubMed  Google Scholar 

  • Takken W, Dekker T, Wijnholds YG (1997) Odor-mediated flight behavior of Anopheles gambiae Giles Sensu Stricto and An. stephensi Liston in response to CO2, acetone, and 1-octen-3-ol (Diptera: Culicidae). J Insect Behav 10:395–407

    Article  Google Scholar 

  • Tasin M, Backman AC, Bengtsson M, Ioriatti C, Witzgall P (2006) Essential host plant cues in the grapevine moth. Naturwissenschaften 93:141–144

    Article  PubMed  CAS  Google Scholar 

  • Tolbert LP, Matsumoto SG, Hildebrand JG (1983) Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. J Neurosci 3:1158–1175

    PubMed  CAS  Google Scholar 

  • Trona F, Anfora G, Bengtsson M, Witzgall P, Ignell R (2010) Coding and interaction of sex pheromone and plant volatile signals in the antennal lobe of the codling moth Cydia pomonella. J Exp Biol 213:4291–4303

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  • Tumlinson JH, Mitchell ER, Doolittle RE, Jackson DM (1994) Field tests of synthetic Manduca sexta sex pheromone. J Chem Ecol 20:579–591

    Article  CAS  Google Scholar 

  • Vickers NJ, Christensen TA, Mustaparta H, Baker TC (1991) Chemical communication in heliothine moths 3. Flight behavior of male Helicoverpa zea and Heliothis virescens in response to varying ratios of intraspecific and interspecific sex-pheromone components. J Comp Physiol A 169:275–280

    Article  Google Scholar 

  • Vickers NJ, Christensen TA, Hildebrand JG (1998) Combinatorial odor discrimination in the brain: attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli. J Comp Neurol 400:35–56

    Article  PubMed  CAS  Google Scholar 

  • Vinje WE, Gallant JL (2000) Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287:1273–1276

    Article  PubMed  CAS  Google Scholar 

  • Visser JH, Avé DA (1978) General green leaf volatiles in the olfactory orientation of the Colorado beetle, Leptinotarsa decemlineata. Entomol Exp Appl 24:738–749

    Article  CAS  Google Scholar 

  • Waldrop B, Christensen TA, Hildebrand JG (1987) GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth, Manduca sexta. J Comp Physiol A 161:23–32

    Article  PubMed  CAS  Google Scholar 

  • Willis MA, Baker TC (1988) Effects of varying sex pheromone component ratios on the zigzagging flight movements of the oriental fruit moth, Grapholita molesta. J Insect Behav 1:357–371

    Article  Google Scholar 

  • Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72:506–519

    Article  PubMed  CAS  Google Scholar 

  • Wu WQ, 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. Proc Natl Acad Sci USA 93:8022–8027

    Article  PubMed  CAS  Google Scholar 

  • Wyatt TD (2010) Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol A 196:685–700

    Article  CAS  Google Scholar 

  • Xu FQ, Greer CA, Shepherd GM (2000) Odor maps in the olfactory bulb. J Comp Neurol 422:489–495

    Article  PubMed  CAS  Google Scholar 

  • Yang CY, Han KS, Boo KS (2009) Sex pheromones and reproductive isolation of three species in genus Adoxophyes. J Chem Ecol 35:342–348

    Article  PubMed  CAS  Google Scholar 

  • Yu YG, Romero R, Lee TS (2005) Preference of sensory neural coding for 1/f signals. Phys Rev Lett 94:103–108

    Google Scholar 

  • Zavada A, Buckley CL, Martinez D, Rospars JP, Nowotny T (2011) Competition-based model of pheromone component ratio detection in the moth. PLoS One 6:e16308

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank E. Constantopoulos for assistance with behavioral experiments, and A. M. Dacks, C. E. Reisenman, A. Beyerlein, and J. M. Fellous for helpful discussion and comments on this work. This research was supported by the National Institute on Deafness and Other Communication Disorders (NIDCD) grants RO1-DC02751 to JGH and NRSA DC97222 to JPM.

Author information

Authors and Affiliations

  1. Department of Biology, Case Western Reserve University, 10900 Euclid Avenue, Cleveland, OH, 44106, USA

    Joshua P. Martin

  2. Department of Neuroscience, University of Arizona, PO Box 210077, Tucson, AZ, 85721, USA

    Hong Lei & John G. Hildebrand

  3. Department of Biology, University of Washington, PO Box 351800, Seattle, WA, 98195, USA

    Jeffrey A. Riffell

Authors
  1. Joshua P. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hong Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffrey A. Riffell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John G. Hildebrand
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joshua P. Martin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martin, J.P., Lei, H., Riffell, J.A. et al. 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 (2013). https://doi.org/10.1007/s00359-013-0849-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-013-0849-z

Keywords

Search

Navigation