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Morphological and physiological properties of pheromone-triggered flipflopping descending interneurons of the male silkworm moth, Bombyx mori

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Abstract

  1. 1.

    The morphology of descending interneurons (DNs) which have arborizations in the lateral accessory lobe (LAL) of the protocerebrum, the higher order olfactory center, and have an axon in the ventral nerve cord (VNC), were characterized in the male silkworm moth, Bombyx mori.

  2. 2.

    Two clusters (group I, group II) of DNs which have arborizations mainly in the LALs were morphologically characterized. The axons of these DNs are restricted to the dorsal part of the each connective (Figs. 1–5).

  3. 3.

    Pheromonal responses of the group I and group II DNs were characterized. Flipflopping activity patterns, which have two distinct firing frequencies (high and low) in response to sequential pheromonal stimulation, were usually recorded (Figs.6–10).

  4. 4.

    Two types of flipflopping activity patterns were classified into those that had an antiphasic relationship (called the ‘FF’ type) between the left and right connectives and those with a synchronized relationship (‘ff’ type) (Figs. 8–12). We propose that some group II DNs show ‘FF’ flipflopping activity patterns (Fig. 10).

  5. 5.

    A state transition was usually elicited by less than 10 ng bombykol, the principal pheromone component. Extra impulses were elicited during constant light stimulation (Fig. 9).

  6. 6.

    Our results suggest that the LAL olfactory pathways might be important for producing flipflopping activity patterns (Fig. 11).

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Abbreviations

AL:

antennal lobe

α:

α-lobe of the mushroom body

AN:

antennal nerve

β:

β-lobe of the mushroom body

Ca:

calyces of the mushroom body

D:

dorsal

DN(s):

descending interneuron(s)

FE:

female equivalent

ff, FF:

flipflopping activity pattern

g:

ordinary glomerulus

L:

lateral

LAL:

lateral accessory lobe

LC:

left connective of the VNC

LH:

lateral horn of the protocerebrum

LLE:

long-lasting excitation

MC:

medial cell cluster of antennal lobe neurons

mgc:

macroglomerular complex

Oe:

oesophageal foramen

OL:

optic lobe

P:

pedunculus

PBN:

protocerebral bilateral neuron

PC:

protocerebrum

RC:

right connective of the VNC

SOG:

suboesophageal ganglion

STIM:

pheromonal stimulation

TES:

N-tris[hydroxymethl]-2-aminoethanesulfonic acid

V:

ventral

VNC:

ventral nerve cord

VP:

ventral protocerebrum

References

  • Arbas EA, Willis MA, Kanzaki R (1993) Organization of goal-oriented locomotion: pheromone-modulated flight behavior of moths. In: Beer RD, Ritzmann RE, McKenna T (eds) Biological neural networks in invertebrate neuroethology and robotics. Academic Press, New York, pp 159–198

    Google Scholar 

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

    Google Scholar 

  • Baker TC (1990) Upwind flight and casting flight: Complementary phasic and tonic systems used for location of sex pheromone sources by male moth. In: Døving KB (ed) Proc 10th Int Symp Olfaction and Taste, Oslo, pp 18–25

  • Butenandt VA, Beckmann R, Stamm D, Hecker E (1959) Über den Sexual-Lockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitution. Z Naturforsch 14b: 283–284

    Google Scholar 

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

    Google Scholar 

  • Homberg U (1987) Structure and functions of the central complex in insects. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure, and functions. Wiley, New York, pp 347–363

    Google Scholar 

  • Homberg U, Kingan TG, Hildebrand JG (1987) Immunocyto-chemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 248: 1–24

    Google Scholar 

  • Homberg U, Würden S, Ircksen H, Rao KR (1991) Comparative anatomy of pigment-dispersing hormone-immunoreactive neuron in the brain of orthopteroid insects. Cell Tissue Res 266: 343–357

    Google Scholar 

  • Kaissling K-E, Kramer E (1990) Sensory basis of pheromone-mediated orientation in moths. Verh Dtsch Zool Ges 83: 109–131

    Google Scholar 

  • Kanzaki R, Shibuya T (1986a) Identification of the deutocerebral neurons responding to the sexual pheromone in the male silkworm moth brain. Zool Sci 3: 409–418

    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, Shibuya T (1992a) Long-lasting excitation of protocerebral bilateral neurons in the pheromone-processing pathways of the male moth Bombyx mori. Brain Res 587: 211–215

    Google Scholar 

  • Kanzaki R, Shibuya T (1992b) Personal computer-based processing technique for analyzing insect mating behavior in response to sex pheromone odor. Sensors and Materials 4: 1–9

    Google Scholar 

  • Kanzaki R, Arbas EA, Hildebrand JG (1991a) Physiology and morphology of protocerebral olfactory neurons in the male moth Manduca sexta. J Comp Physiol A 168: 281–298

    Google Scholar 

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

    Google Scholar 

  • Kanzaki R, Sugi N, Shibuya T (1992) Self-generated zigzag turning of Bombyx mori males during pheromone-mediated upwind walking. Zool Sci 9: 515–527

    Google Scholar 

  • Kennedy JS (1983) Zigzagging and casting as a programmed response to wind-borne odour: a review. Physiol Entomol 8: 109–120

    Google Scholar 

  • Koontz MA, Schneider D (1987) Sexual dimorphism in neuronal projections from the antennae of silk moths (Bombyx mori, Antheraea polyphemus) and the gypsy moth (Lymantria dispar). Cell Tissue Res 249: 39–50

    Google Scholar 

  • Kramer E (1975) Orientation of the male silkmoth to the sex attractant bombykol. In: Denton DA, Coghlan JP (eds) Olfaction and taste V. Academic Press, New York, pp 329–335

    Google Scholar 

  • Kramer E (1986) Turbulent diffusion and pheromone-triggered anemotaxis. In: Payne TL, Birch MC, Kennedy CEJ (eds) Mechanisms in insect olfaction. Oxford University Press, Oxford, pp 59–67

    Google Scholar 

  • Light DM (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 

  • Meyer CS, Lynn DK, Hamilton DJ (1968) Analysis and design of integrated circuits. McGraw-Hill Book Company, New York St. Louis San Francisco Toronto London Sydney

    Google Scholar 

  • Obara Y (1979) Bombyx mori mating dance: an essential in locating the female. Appl Entomol Zool 14: 130–132

    Article  Google Scholar 

  • Olberg RM (1983a) Pheromone-triggered flip-flopping interneurons in the ventral nerve cord of the silkworm moth, Bombyx mori. J Comp Physiol 152: 297–307

    Google Scholar 

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

    Google Scholar 

  • Olberg RM, Willis MA (1990) Pheromone modulated optomotor response in male gypsy moths, Lymantria dispar L.: Directionally selective visual interneurons in the ventral nerve cord. J Comp Physiol A 167: 707–714

    Google Scholar 

  • Sasaki M, Riddiford LM (1984) Regulation of reproductive behavior and egg maturation in the tobacco hawk moth, Manduca sexta. Physiol Entomol 9: 315–327

    Google Scholar 

  • Schildberger K (1981) Some physiological features of mushroombody linked fibers in the house cricket brain. Naturwissenschaften 67: 623–624

    Google Scholar 

  • Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26: 31–43

    CAS  PubMed  Google Scholar 

  • Strauß R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13: 1852–1861

    Google Scholar 

  • Willis MA, Arbas EA (1991) Odor-modulated upwind flight of the sphinx moth Manduca sexta. J Comp Physiol A 169: 427–440

    Google Scholar 

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Authors and Affiliations

  1. Institute of Biological Sciences, University of Tsukuba, Tsukuba, 305, Ibaraki, Japan

    R. Kanzaki, A. Ikeda & T. Shibuya

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  1. R. Kanzaki
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  2. A. Ikeda
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  3. T. Shibuya
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Kanzaki, R., Ikeda, A. & Shibuya, T. Morphological and physiological properties of pheromone-triggered flipflopping descending interneurons of the male silkworm moth, Bombyx mori . J Comp Physiol A 175, 1–14 (1994). https://doi.org/10.1007/BF00217431

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