Skip to main content
Log in

Physiology and morphology of descending neurons in pheromone-processing olfactory pathways in the male moth Manduca sexta

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

Summary

  1. 1.

    We have characterized the responses and structure of olfactory descending neurons (DNs) that reside in the protocerebrum (PC) of the brain of male sphinx moths Manduca sexta and project toward thoracic ganglia.

  2. 2.

    Excitatory responses of DNs to pheromone blends were of two general types: (a) brief excitation (BE) that recovered to background in <1 s after the stimulus, and (b) long-lasting excitation (LLE) that outlasted the stimulus by ≥1 s and, in many cases, as long as 30 s. Individual pheromone components were ineffective in eliciting LLE.

  3. 3.

    Some neurons showing LLE also exhibited state-dependent responses to pheromonal stimuli. When such neurons were in a state of low background firing, stimulation with pheromone blend elicited LLE. When they were in a state of LLE, an identical stimulus reduced firing for 5–10 s after which firing gradually increased to the initial higher level.

  4. 4.

    Thirteen stained DNs were reconstructed from serial sections for detailed analysis of their morphology in the brain. DNs exhibiting LLE had neurites concentrated in the lateral accessory lobes (LALs) in the protocerebrum and adjacent neuropil. Most DNs exhibiting only BE to pheromonal stimuli and other DNs showing responses only to visual or mechanosensory stimuli did not have branches in the LALs.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AL :

antennal lobe

aL α :

lobe of the mushroom body

AMMC :

antennal motor and mechanosensory center

BE :

brief excitation

bL β :

lobe of the mushroom body

Ca :

primary calyces of the mushroom body

CB :

central body

DN :

descending neuron

FE :

female equivalent

IACT :

inner antenno-cerebral tract

L :

lateral

LAL :

lateral accessory lobe

LLE :

long-lasting excitation

MB :

mushroom body

OACT :

uter antenno-cerebral tract

Oe :

oesophageal foramen

P :

pedunculus

PC :

protocerebrum

PCN :

protocerebral neuron

SOG :

suboesophageal ganglion

LY :

Lucifer Yellow CH

TES :

N-trishydroxymethyl]methyl-2-aminoethanesulfonic acid

VNC :

ventral nerve cord

YL :

Y-lobe of the mushroom body

References

  • Arbas EA, Calabrese RL (1984) Rate modification in the heartbeat central pattern generator of the medicinal leech. J Comp Physiol A 155:783–794

    Google Scholar 

  • Arbas EA, Kanzaki R, Hildebrand JG (1990) State-dependent activity changes in descending neurons in olfactory pathways of Manduca sexta. Soc Neurosci Abstr 16:758

    Google Scholar 

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

  • Boeckh J, Ernst K-D (1987) Contribution of single unit analysis in insects to an understanding of olfactory function. J Comp Physiol A 161:549–565

    Google Scholar 

  • Brodfuehrer PD, Friesen WO (1986) Initiation of swimming activity by trigger neurons in the leech subesophageal ganglion I. Output connections of Tr1 and Tr2. J Comp Physiol A 159:489–502

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Derby CD, Blaustein DN (1988) Morphological and physiological characterization of individual olfactory interneurons connecting the brain and eyestalk ganglia of the crayfish. J Comp Physiol A 163:777–794

    Google Scholar 

  • Dickinson PS, Nagy F (1983) Control of a central pattern generator by an identified modulatory interneurone in Crustacea II. Induction and modification of plateau properties in pyloric neurones. J Exp Biol 105:59–82

    Google Scholar 

  • Hamilton KA, Ache BW (1983) Olfactory excitation of interneurons in the brain of the spiny lobster. J Comp Physiol 150:129–140

    Google Scholar 

  • Hensler K (1989) Corrective flight steering in locusts: Convergence of extero- and proprioceptive inputs in descending deviation detectors. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum Press, New York, pp 531–544

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    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 

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

    Google Scholar 

  • Kanzaki R (1989) Physiology and morphology of higher-order neurons in olfactory pathways of the moth brain: Pheromone-processing neurons in the protocerebrum. In: Erber J, Menzel R, Pflüger HJ, Todt D (eds) Neural mechanisms of behavior. Proc 2nd Int Congress Neuroethology. G. Thieme, Stuttgart New York, pp 253–254

    Google Scholar 

  • Kanzaki R, Arbas EA (1990) Olfactory and visual influences on fictive flight in Manduca sexta. Soc Neurosci Abstr 16:758

    Google Scholar 

  • Kanzaki R, Shibuya T (1986) 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 

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

    Google Scholar 

  • Katz PS, Harris-Warrick RM (1989) Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. II. Rapid nicotinic and prolonged modulatory effects on neurons in the stomatogastric ganglion. J Neurophysiol 62:571–581

    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 

  • Lehman HK (1990) Circadian control of Manduca sexta flight. Soc Neurosci Abstr 16:1334

    Google Scholar 

  • Lennard PR, Getting PA, Hume RI (1980) Central pattern generator mediating swimming in Tritonia. II. Initiation, maintenance, and termination. J Neurophysiol 44:165–173

    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) Pheromone-triggered flip-flopping interneurons in the ventral nerve cord of the silkworm moth, Bombyx mori. J Comp Physiol A 152:297–307

    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 

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

    Google Scholar 

  • Schneiderman AM, Hildebrand JG, Brennan MM, Tumlinson JH (1986) Trans-sexually grafted antennae alter pheromone-directed behaviour in a moth. Nature 323:801–803

    Google Scholar 

  • Schweitzer ES, Sanes JR, Hildebrand JG (1976) Ontogeny of electroantennogram responses in the moth, Manduca sexta. J Insect Physiol 22:955–960

    Google Scholar 

  • Starratt AM, Dahm KH, Allen N, Hildebrand JG, Payne TL, Roller H (1978) Bombykal, a sex pheromone of the sphinx moth, Manduca sexta. Z Naturforsch 34C:9–12

    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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Weeks JC, Kristan WB Jr (1978) Initiation, maintenance and modulation of swimming in the medicinal leech by the activity of a single neurone. J Exp Biol 77:71–88

    Google Scholar 

  • Wiersma CAG, Yanagisawa K (1971) On types of interneurons responding to visual stimulation present in the optic nerve of the rock lobster, Panulirus interruptus. J Neurobiol 2:291–309

    Google Scholar 

  • Wiersma CAG, York B (1972) Properties of the seeing fibers in the rock lobster: Field structure, habituation, attention and distraction. Vision Res 12:627–640

    Google Scholar 

  • Williamson R, Burns MD (1982) Large neurones in locust neck connectives. J Comp Physiol 147:379–388

    Google Scholar 

  • Willis MA, Arbas EA (1990) Odor-mediated upwind flight behavior of the tobacco hornworm moth Manduca sexta. Soc Neurosci Abstr 16:757

    Google Scholar 

  • Willis MA, Arbas EA (1991) Odor-modulated upwind flight behavior of the tobacco hornworm moth Manduca sexta. J Comp Physiol A, In press

  • Willows AOD, Lloyd PE, Masinovsy BP (1988) Multiple transmitter neurons in Tritonia III. Modulation of central pattern generator controlling feeding. J Neurobiol 19:69–86

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kanzaki, R., Arbas, E.A. & Hildebrand, J.G. Physiology and morphology of descending neurons in pheromone-processing olfactory pathways in the male moth Manduca sexta . J Comp Physiol A 169, 1–14 (1991). https://doi.org/10.1007/BF00198168

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00198168

Key words

Navigation