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Olfactory interneurons in the brain of the larval sphinx moth Manduca sexta

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Summary

  1. 1.

    The physiology and morphology of olfactory interneurons in the brain of larval Manduca sexta were studied using intracellular recording and staining techniques. Antennal olfactory receptors were stimulated with volatile substances from plants and with pure odorants. Neurons responding to the stimuli were investigated further to reveal their response specificities, dose-response characteristics, and morphology.

  2. 2.

    We found no evidence of specific ‘labeled-lines’ among the odor-responsive interneurons, as none responded exclusively to one plant odor or pure odorant; most olfactory interneurons were broadly tuned in their response spectra. This finding is consistent with an ‘across-fiber’ pattern of odor coding.

  3. 3.

    Mechanosensory and olfactory information are integrated at early stages of central processing, appearing in the responses of some local interneurons restricted to the primary olfactory nucleus in the brain, the larval antennal center (LAC).

  4. 4.

    The responses of LAC projection neurons and higher-order protocerebral interneurons to a given odor were more consistent than the responses of LAC local interneurons.

  5. 5.

    The LAC appears to be functionally subdivided, as both local and projection neurons had arborizations in specific parts of the LAC, but none had dendrites throughout the LAC.

  6. 6.

    The mushroom bodies and the lateral protocerebrum contain neurons that respond to olfactory stimulation.

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Abbreviations

BAL :

bombykal

CNS :

central nervous system

E2H :

(E)-2-hexenal

KAc :

potassium acetate

LAC :

larval antennal center

LY :

Lucifer Yellow CH

MGC :

macroglomerular complex

SEM :

standard error of the mean

References

  • Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurons in wholemount preparations. Brain Res 138:359–363

    Google Scholar 

  • Baker EA (1982) Chemistry and morphology of plant epicuticular waxes. In: Cutler DF, Alvin KF, Price CE (eds) The plant cuticle. Linnaean Society Symposium Series No. 10. Academic Press, New York, pp 139–165

    Google Scholar 

  • Barbosa P, Greenblatt J, Withers W, Cranshaw W, Harrington EA (1979) Host-plant preferences and their induction in larvae of the gypsy moth, Lymantria dispar. Entomol Exp Appl 26:180–188

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Boeckh J, Sandri C, Akert K (1970) Sensorische Eingänge und synaptische Verbindungen im Zentralnervensystem von Insekten. Z Zellforsch 103:429–446

    Google Scholar 

  • Boeckh J, Ernst KD, Sass H, Waldow U (1984) Anatomical and physiological characteristics of individual neurones in the central antennal pathways of insects. J Insect Physiol 30:15–26

    Google Scholar 

  • Burrows M, Boeckh J, Esslen J (1982) Physiological and morphological properties of interneurons in the deutocerebrum of male cockroaches which respond to female pheromone. J Comp Physiol 145:447–457

    Google Scholar 

  • Calabrese RL (1980) Control of multiple impulse-initiation sites in a leech interneuron. J Neurophysiol 44:878–896

    Google Scholar 

  • Calabrese RL, Kennedy D (1974) Multiple sites of spike initiation in a single dendritic system. Brain Res 83:316–321

    Google Scholar 

  • Camazine SM, Hildebrand JG (1979) Central projections of antennal sensory neurons in mature and developing Manduca sexta. Soc Neurosci Abstr 5:155

    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

    Google Scholar 

  • Christensen TA, Hildebrand JG (1987b) Functions, organization, and physiology of the olfactory pathways in the lepidopteran brain. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure, and function. John Wiley and Sons, New York, pp 457–484

    Google Scholar 

  • Christensen TA, Hildebrand JG (1988) Frequency coding by central olfactory neurons in the sphinx moth Manduca sexta. Chem Senses 13:123–130

    Google Scholar 

  • Christensen TA, Mustaparta H, Hildebrand JG (1989) Discrimination of sex pheromone blends in the olfactory system of the moth. Chem Senses 14:202

    Google Scholar 

  • De Boer G, Hanson FE (1984) Foodplant selection and induction of feeding preference among host and non-host plants in larvae of the tobacco hornworm, Manduca sexta. Entomol Exp Appl 35:177–193

    Google Scholar 

  • De Boer G, Hanson FE (1987) Differentiation of roles of chemosensory organs in food discrimination among host and non-host plants by larvae of the tobacco hornworm. Physiol Entomol 12:387–398

    Google Scholar 

  • De Jong R, Visser JH (1988) Integration of olfactory information in the Colorado potato beetle brain. Brain Res 447:10–17

    Google Scholar 

  • Dethier VG (1937) Gustation and olfaction in lepidopterous larvae. Biol Bull 72:7–23

    Google Scholar 

  • Dethier VG (1941) The function of antennal receptors in lepidopterous larvae. Biol Bull 80:403–414

    Google Scholar 

  • Dethier VG (1967) Feeding and drinking behavior of invertebrates. In: Code CF (ed) Handbook of physiology, Sec B. Alimentary canal. Am Physiol Assn, Washington DC, vol 1, pp 79–96

    Google Scholar 

  • Dethier VG (1980) Responses of some olfactory receptors of the eastern tent caterpillar (Malacosoma americanum) to leaves. J Chem Ecol 6:213–220

    Google Scholar 

  • Dethier VG, Crnjar RM (1982) Candidate codes in the gustatory system of caterpillars. J Gen Physiol 79:543–569

    Google Scholar 

  • Dethier VG, Kuch JH (1971) Electrophysiological studies of gustation in lepidopterous larvae. I. Comparative sensitivity to sugars, amino acids, and glycosides. Z Vergl Physiol 72:343–363

    Google Scholar 

  • Dethier VG, Schoonhoven LM (1969) Olfactory coding by lepidopterous larvae. Entomol Exp Appl 12:535–543

    Google Scholar 

  • Erber J (1978) Response characteristics and after-effects of multimodal neurones in the mushroom body area of the honeybee. Physiol Entomol 3:77–89

    Google Scholar 

  • Erber J, Masuhr T, Menzel R (1980) Localization of short-term memory in the brain of the honeybee Apis mellifera. Physiol Entomol 5:343–358

    Google Scholar 

  • Ernst K-D, Boeckh J (1983) A neuroanatomical study on the organisation of the central antennal pathway in insects. III. Neuroanatomical characterization of physiologically defined response types of deutocerebral neurons in Periplaneta americana. Cell Tissue Res 229:1–22

    Google Scholar 

  • Hanson FE, Dethier VG (1973) Role of gustation and olfaction in food plant discrimination in the tobacco hornworm, Manduca sexta. J Insect Physiol 19:1019–1034

    Google Scholar 

  • Heitler WJ, Goodman CS (1978) Multiple sites of spike initiation in a bifurcating locust neurone. J Exp Biol 76:63–84

    Google Scholar 

  • Homberg U (1981) Ableitungen und Lucifer Yellow Markierungen von Neuronen des Tractus olfactorio-globularis im Bienengehirn. Verh Dt Zool Ges 74:176

    Google Scholar 

  • Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A 154:825–836

    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

    Google Scholar 

  • Hoskins SG, Homberg U, Kingan TG, Hildebrand JG (1986) Immunocytochemistry of GABA in the antennal lobes of the sphinx moth, Manduca sexta. Cell Tissue Res 244:243–252

    Google Scholar 

  • Humason GL (1967) Animal tissue techniques. 2nd ed. Freeman, San Francisco

    Google Scholar 

  • Itagaki H, Hildebrand JG (1986) Central processing of olfactory information in the brain of the larval tobacco hornworm. Soc Neurosci Abstr 12:857

    Google Scholar 

  • Itagaki H, Hildebrand JG (1988) Responses of olfactory interneurons in the brain of larval Manduca sexta. Soc Neurosci Abstr 14:380

    Google Scholar 

  • Jermy T, Hanson FE, Dethier VG (1968) Induction of specific food preference in lepidopterous larvae. Entomol Exp Appl 11:211–230

    Google Scholar 

  • Kanzaki R, Shibuya T (1984) Identification and pheromone responses of the mushroom body neurons in the male silkworm moth, Bombyx mori. Zool Sci 1:878

    Google Scholar 

  • Kanzaki R, Shibuya T (1986a) Identification of deutocerebral neurons responding to the sexual pheromone in the male silkworm moth brain. Zool Sci 3:409–413

    Google Scholar 

  • Kanzaki R, Shibuya T (1986b) Descending protocerebral neurons related to the mating dance of the male silkworm moth. Brain Res 377:378–382

    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

    Google Scholar 

  • Kent KS (1985) Metamorphosis of the antennal center and the influence of sensory innervation on the formation of glomeruli in the hawkmoth Manduca sexta. PhD Dissertation, Harvard University, Cambridge, USA

    Google Scholar 

  • Kent KS, Hildebrand JG (1987) Cephalic sensory pathways in the central nervous system of larval Manduca sexta (Lepidoptera: Sphingidae). Phil Trans R Soc Lond B 315:1–36

    Google Scholar 

  • Kent KS, Hoskins SG, Hildebrand JG (1987) A novel serotoninimmunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life. J Neurobiol 18:451–465

    Google Scholar 

  • Lazar G (1978) Application of cobalt-filling technique to retinal projections in the frog. Neuroscience 3:725–736

    Google Scholar 

  • Light D (1986) Central integration of sensory signals: An exploration of processing of pheromonal and multimodal information in lepidopteran brains. In: Payne TL, Birch MC, Kennedy CEJ (eds) Mechanisms in insect olfaction. Oxford University Press, Oxford, pp 287–301

    Google Scholar 

  • Llinás R, Nicholson C (1971) Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J Neurophysiol 34:532–551

    Google Scholar 

  • Llinás R, Nicholson C, Freeman JA, Hillman DE (1968) Dendritic spikes and their inhibition in alligator Purkinje cells. Science 160:1132–1135

    Google Scholar 

  • Ma WC (1972) Dynamics of feeding responses in Pieris brassicae Linn. as a function of chemosensory input: A behavioural, ultrastructural and electrophysiological study. Med Landbouwhogeschool Wag 72–11:1–162

    Google Scholar 

  • Ma WC (1976) Mouth parts and receptors involved in feeding behaviour and sugar perception in the African armyworm Spodoptera exempta (Lepidoptera: Noctuidae). Symp Biol Hung 16:139–151

    Google Scholar 

  • Marder E, Eisen JS (1984) Transmitter identification of pyloric neurons: Electrically coupled neurons use different transmitters. J Neurophysiol 51:1345–1361

    Google Scholar 

  • Martin JT, Juniper BE (1970) The cuticle of plants. St Martin's Press, New York, 347 pp

    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

    Google Scholar 

  • Olberg RM (1983) Interneurons sensitive to female pheromone in the deutocerebrum of the male silkworm moth, Bombyx mori. Physiol Entomol 8:419–428

    Google Scholar 

  • Pichon Y, Satelle 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

    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 56C: 77–84

    Google Scholar 

  • Randolph PW, Itagaki H (1989) Central projections of cephalic sensory neurons in the larvae of Heliothis moths. Soc Neurosci Abstr 15:1290

    Google Scholar 

  • Sandeman DC (1969a) The site of synaptic activity and impulse initiation in an identified motoneurone in the crab brain. J Exp Biol 50:771–784

    Google Scholar 

  • Sandeman DC (1969b) Integrative properties of a reflex motoneurone in the brain of the crab Carcinus maenas. Z Vergl Physiol 64:450–464

    Google Scholar 

  • Sanes JR, Hildebrand JG (1976a) Structure and development of antennae in a moth, Manduca sexta. Dev Biol 151:282–299

    Google Scholar 

  • Sanes JR, Hildebrand JG (1976b) Origin and morphogenesis of sensory neurons in an insect antenna. Dev Biol 51:300–319

    Google Scholar 

  • Saxena KN, Schoonhoven LM (1978) Induction of orientational and feeding preferences in Manduca sexta larvae for an artificial diet containing citral. Entomol Exp Appl 23:173–180

    Google Scholar 

  • Saxena KN, Schoonhoven LM (1982) Induction of orientational and feeding preferences in Manduca sexta larvae for different food sources. Entomol Exp Appl 32:173–180

    Google Scholar 

  • Schildberger K (1984) Multimodal interneurons in the cricket brain: Properties of identified extrinsic mushroom body cells. J Comp Physiol A 154:71–79

    Google Scholar 

  • Schoonhoven LM (1969) Gustation and foodplant selection in some lepidopterous larvae. Entomol Exp Appl 12:555–564

    Google Scholar 

  • Schoonhoven LM (1986) What makes a caterpillar eat? The sensory code underlying feeding behavior. In: Chapman RF, Bernays EA, Stoffolano JG Jr (eds) Perspectives in chemoreception and behavior. Springer, Berlin Heidelberg New York, pp 79–97

    Google Scholar 

  • Schoonhoven LM, Dethier VG (1966) Sensory aspects of hostplant discrimination by lepidopterous larvae. Arch Néerl Zool 16:497–530

    Google Scholar 

  • Selzer LS (1984) Physiology and morphology of the larval sexual pheromone-sensitive neurones in the olfactory lobe of the cockroach, Periplaneta americana. J Insect Physiol 30:537–546

    Google Scholar 

  • Selzer R (1979) Morphological and physiological identification of food odour-specific neurones in the deutocerebrum of Periplaneta americana. J Comp Physiol 134:159–163

    Google Scholar 

  • Städler E, Hanson FE (1975) Olfactory capabilities of the ‘gustatory’ chemoreceptors of the tobacco hornworm larvae. J Comp Physiol 104:97–102

    Google Scholar 

  • Starratt AN, Dahm KH, Allen N, Hildebrand JG, Payne TL, Röller H (1979) Bombykal, a sex pheromone of the sphinx moth Manduca sexta. Z Naturforsch 34c:9–12

    Google Scholar 

  • Stewart WW (1978) Functional connections between cells revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759

    Google Scholar 

  • Stocker RF, Singh RN, Schorderet M, Siddiqi O (1983) Projection patterns of different types of antennal sensilla in the antennal glomeruli of Drosophila melanogaster. Cell Tissue Res 232:237

    Google Scholar 

  • Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York 214 pp

    Google Scholar 

  • Strausfeld NJ, Seyan HS (1985) Convergence of visual, haltere and prosternal inputs at weak motor neurons of Calliphora. Cell Tissue Res 240:1–16

    Google Scholar 

  • Suzuki H, Tateda H, Kuwabara M (1976) Activities of antennal and ocellar interneurons in the protocerebrum of the honeybee. J Exp Biol 64:405–418

    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

    Google Scholar 

  • Visser JH (1983) Differential sensory perception of plant compounds by insects. In: Hedin PA (ed) Plant resistance to insects. ACS Symposium Series, vol 208, pp 215–230

  • Waldow U (1977) CNS units in cockroach (Periplaneta americana): Specificity of response to pheromones and other odor stimuli. J Comp Physiol 116:1–17

    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

    Google Scholar 

  • Westerfield M, Joyner RW, Moore JW (1978) Temperature-sensitive conduction failure at axon branch points. J Neurophysiol 41:1–8

    Google Scholar 

  • Wigglesworth VB (1957) Use of osmium in the fixation and staining of tissues. Proc R Soc Lond B 147:185–199

    Google Scholar 

  • Yamamoto RT, Fraenkel GS (1960) The specificity of the tobacco hornworm, Protoparce sexta, to solanaceous plants. Ann Entomol Soc Am 53:503–507

    Google Scholar 

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  1. H. Itagaki

    Present address: Dept. of Biology, Kenyon College, 43022, Gambier, OH, USA

Authors and Affiliations

  1. Arizona Research Laboratories Division of Neurobiology, University of Arizona, 611 Gould-Simpson Bldg., 85721, Tucson, AZ, USA

    H. Itagaki & J. G. Hildebrand

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Itagaki, H., Hildebrand, J.G. Olfactory interneurons in the brain of the larval sphinx moth Manduca sexta . J Comp Physiol A 167, 309–320 (1990). https://doi.org/10.1007/BF00192566

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