Skip to main content
Log in

Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx mothManduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Using an antiserum against the tetrapeptide FMRFamide, we have studied the distribution of FMRFamide-like substances in the brain and suboesophageal ganglion of the sphinx mothManduca sexta. More than 2000 neurons per hemisphere exhibit FMRFamide-like immunoreactivity. Most of these cells reside within the optic lobe. Particular types of FMRFamide-immunoreactive neurons can be identified. Among these are neurosecretory cells, putatively centrifugal neurons of the optic lobe, local interneurons of the antennal lobe, mushroom-body Kenyon cells, and small-field neurons of the central complex. In the suboesophageal ganglion, groups of ventral midline neurons exhibit FMRFamide-like immunoreactivity. Some of these cells have axons in the maxillary nerves and apparently give rise to FMRFamide-immunoreactive terminals in the sheath of the suboesophageal ganglion and the maxillary nerves. In local interneurons of the antennal lobe and a particular group of protocerebral neurons, FMRFamide-like immunoreactivity is colocalized with GABA-like immunoreactivity. This suggests that FMRFamide-like peptides may be cotransmitters of these putatively GABAergic interneurons. All FMRFamide-immunoreactive neurons are, furthermore, immunoreactive with an antiserum against bovine pancreatic polypeptide, and the vast majority is also immunoreactive with an antibody against the molluscan small cardioactive peptide SCPB. Therefore, it is possible that more than one peptide is localized within many FMRFamide-immunoreactive neurons. The results suggest that FMRFamide-related peptides are widespread within the nervous system ofM. sexta and might function as neurohormones and neurotransmitters in a variety of neuronal cell types.

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.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AL :

antennal lobe

BPPLI :

bovine pancreatic polypeptide-like immunoreactivity

FLI :

FMRFamide-like immunoreactivity

GLI :

GABA-like immunoreactivity

NSC :

neurosecretory cell

SCP B LI :

small cardioactive peptideB-like immunoreactivity

SLI :

serotonin-like immunoreactivity

SOG :

suboesophageal ganglion

References

  • Adams ME, O'Shea M (1983) Peptide cotransmitter at a neuromuscular junction. Science 221:286–289

    PubMed  Google Scholar 

  • Bausenwein B (1988) Neuronale Aktivitätsmarkierung während visueller Flugsteuerung vonDrosophila melanogaster. Doctoral Dissertation, University of Würzburg

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

    Google Scholar 

  • Bicker G, Schäfer S, Ottersen OP, Storm-Mathisen J (1988) Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems. J Neurosci 8:2108–2122

    PubMed  Google Scholar 

  • Boer HH, Schot LPC, Roubos EW, terMaat A, Lodder JC, Reichelt D, Swaab DF (1979) ACTH-like immunoreactivity in two electrotonically coupled giant neurons in the pond snailLymnea stagnalis. Cell Tissue Res 202:231–240

    PubMed  Google Scholar 

  • Brezina V, Eckert R, Erxleben C (1987a) Modulation of potassium conductances by an endogenous neuropeptide in neurones ofAplysia californica. J Physiol (Lond) 382:267–290

    Google Scholar 

  • Brezina V, Eckert R, Erxleben C (1987b) Suppression of calcium current by an endogenous neuropeptide in neurons ofAplysia californica. J Physiol (Lond) 388:565–595

    Google Scholar 

  • Brown MR, Lea AO (1988) FMRFamide- and adipokinetic hormone-like immunoreactivity in the nervous system of the mosquitoAedes aegypti. J Comp Neurol 270:606–614

    PubMed  Google Scholar 

  • Callaway JC, Masinovsky B, Graubard K (1987) Co-localization of SCPB-like and FMRFamide-like immunoreactivities in crustacean nervous system. Brain Res 405:295–304

    PubMed  Google Scholar 

  • Carroll LS, Carrow GM, Calabrese RL (1986) Localization and release of FMRFamide-like immunoreactivity in the cerebral neuroendocrine system ofManduca sexta. J Exp Biol 126:1–14

    PubMed  Google Scholar 

  • Colombaioni L, Paupardin-Tritsch D, Vidal PP, Gerschenfeld HM (1985) The neuropeptide FMRFamide decreases both the Ca+ conductance and a cyclic 3′,5′-adenosine monophosphate-dependent K+ conductance in identified molluscan neurons. J Neurosci 5:2533–2538

    PubMed  Google Scholar 

  • Copenhaver PF, Truman JW (1986) Metamorphosis of the cerebral neuroendocrine system in the mothManduca sexta. J Comp Neurol 249:186–204

    PubMed  Google Scholar 

  • Cottrell GA, Davies NW, Turner J, Oates A (1988) Actions and roles of FMRFamide peptides inHelix. In: Thorndyke MC, Goldsworthy GJ (eds) Neurohormones in invertebrates. Cambridge University Press, Cambridge, pp 283–298

    Google Scholar 

  • Cropper EC, Lloyd PE, Reed W, Tenenbaum R, Kupfermann I, Weiss KR (1987) Multiple neuropeptides in cholinergic motoneurons ofAplysia: Evidence for modulation intrinsic to the motor circuit. Proc Natl Acad Sci USA 84:3486–3490

    PubMed  Google Scholar 

  • Dockray GJ, Reeve JR Jr, Shively J, Gayton RJ, Barnard CS (1983) A novel active pentapeptide from chicken brain identified by antibodies to FMRFamide. Nature 305:328–330

    PubMed  Google Scholar 

  • Ebberink RHM, Price DA, Loenhout H van, Doble KE, Riehm JP, Geraerts WPM, Greenberg MJ (1987) The brain ofLymnea contains a family of FMRFamide-like peptides. Peptides 8:515–522

    PubMed  Google Scholar 

  • Evans PD, Myers CM (1986a) Peptidergic and aminergic modulation of insect skeletal muscle. J Exp Biol 124:143–176

    Google Scholar 

  • Evans PD, Myers CM (1986b) The modulatory actions of FMRFamide and related peptides on locust skeletal muscle. J Exp Biol 126:403–422

    Google Scholar 

  • Furness JB, Costa M, Emson OC, Håkanson R, Moghimzadeh E, Sundler F, Taylor IL, Chance RE (1983) Distribution, pathways and reactions to drug treatment of nerves with neuropeptide Y- and pancreatic polypeptide-like immunoreactivity in the guinea-pig digestive tract. Cell Tissue Res 234:71–92

    PubMed  Google Scholar 

  • Greenberg MJ (1983) The responsiveness of molluscan muscles to FMRFamide, its analogs and other neuropeptides. In: Lever J, Boer HH (eds) Molluscan neuro-endocrinology. North Holland Publishing, Amsterdam, pp 190–195

    Google Scholar 

  • Hanesch U, Fischbach K-F, Heisenberg M (1989) Neuronal architecture of the central complex inDrosophila melanogaster. Cell Tissue Res 257:343–366

    Google Scholar 

  • Hökfelt T, Fuxe K, Pernow B (1986) Coexistence of neuronal messengers: A new principle in chemical transmission. Progress in brain research vol 68. Elsevier, Amsterdam

    Google Scholar 

  • Holman GM, Cook BJ, Nachman RJ (1986) Isolation, primary structure and synthesis of leucomyosuppressin, an insect neuropeptide that inhibits spontaneous contractions of the cockroach hindgut. Comp Biochem Physiol 85C:329–333

    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 347–367

    Google Scholar 

  • Homberg U, Hildebrand JG (1989a) Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx mothManduca sexta. Cell Tissue Res 258:1–24

    PubMed  Google Scholar 

  • Homberg U, Hildebrand JG (1989b) Serotonin-immunoreactivity in the optic lobes of the sphinx mothManduca sexta and colocalization with FMRFamide- and SCPB-immunoreactivity. J Comp Neurol 288:243–253

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Ichinose M, McAdoo DJ (1988) The voltage-dependent, slow inward current induced by the neuropeptide FMRFamide inAplysia neuron R14. J Neurosci 8:3891–3900

    PubMed  Google Scholar 

  • Kingan TG, Homberg U, Hildebrand JG (1987) The distribution and characterization of FMRFamide-like peptides in the brain of the mothManduca sexta. Soc Neurosci Abstr 13:234

    Google Scholar 

  • Kingan TG, Teplow DB, Hildebrand JG, Hanneman EH, Rao KR, Kammer AE, Jardine I, Hunt DF (1989) Characterization of a new peptide in the FMRFamide family from the CNS of the hawkmoth,Manduca sexta. Soc Neurosci Abstr 15:26

    Google Scholar 

  • Kobierski LA, Beltz BS, Trimmer BA, Kravitz EA (1987) FMRFamidelike peptides ofHomarus americanus: Distribution, immunocytochemical mapping, and ultrastructural localization in terminal varicosities. J Comp Neurol 266:1–15

    PubMed  Google Scholar 

  • Kuhlman JR, Li C, Calabrese RL (1985a) FMRFamide-like substance in the leech. I. Immunocytochemical localization. J Neurosci 5:2301–2309

    PubMed  Google Scholar 

  • Kuhlman JR, Li C, Calabrese RL (1985b) FMRFamide-like substances in the leech. II. Bioactivity on the heartbeat system. J Neurosci 5:2310–2317

    PubMed  Google Scholar 

  • Lehman HK, Greenberg MJ (1987) The actions of FMRFamidelike peptides on visceral and somatic muscles of the snailHelisoma aspersa. J Exp Biol 131:55–68

    PubMed  Google Scholar 

  • Li C, Calabrese RL (1987) FMRFamide-like substances in the leech. III. Biochemical characterization and physiological effects. J Neurosci 7:595–603

    PubMed  Google Scholar 

  • Lloyd PE, Frankfurt M, Stevens P, Kupfermann I, Weiss KR (1987) Biochemical and immunocytochemical localization of the neuropeptides FMRFamide, SCPA, SCPB to neurons involved in the regulation of feeding inAplysia. J Neurosci 7:1123–1132

    PubMed  Google Scholar 

  • Marder E, Calabrese RL, Nusbaum MP, Trimmer B (1987) Distribution and partial characterization of FMRFamide-like peptides in the stomatogastric nervous system of the rock crab,Cancer borealis, and the spiny lobster,Panulirus interruptus. J Comp Neurol 259:150–163

    PubMed  Google Scholar 

  • Masinovsky B, Kempf SC, Callaway JC, Willows AOD (1988) Monoclonal antibodies to the molluscan small cardioactive peptide SCPB: Immunolabeling of neurons in diverse invertebrates. J Comp Neurol 273:500–512

    PubMed  Google Scholar 

  • Mercer AR, Mobbs PG, Davenport AP, Evans PD (1983) Biogenic amines in the brain of the honeybee,Apis mellifera. Cell Tissue Res 234:655–677

    PubMed  Google Scholar 

  • Meyrand P, Golowasch J, Marder E (1987) FMRFamide and related peptides switch a crustacean muscle into an oscillatory mode. Soc Neurosci Abstr 13:1256

    Google Scholar 

  • Milde JJ (1988) Visual responses of interneurones in the posterior median protocerebrum and the central complex of the honeybeeApis mellifera. J Insect Physiol 34:427–436

    Google Scholar 

  • Mobbs PG (1985) Brain structure. In Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol V. Pergamon, Oxford, pp 299–370

    Google Scholar 

  • Murphy AD, Lukowiak K, Stell WK (1985) Peptidergic modulation of patterned motor activity in identified neurons ofHelisoma. Proc Natl Acad Sci USA 82:7140–7144

    Google Scholar 

  • Myers CM, Evans PD (1985a) The distribution of bovine pancreatic polypeptide/FMRFamide-like immunoreactivity in the ventral nervous system of the locust. J Comp Neurol 234:1–16

    PubMed  Google Scholar 

  • Myers CM, Evans PD (1985b) An FMRFamide antiserum differentiates between populations of antigens in the ventral nervous system of the locust,Schistocerca gregaria. Cell Tissue Res 242:109–114

    Google Scholar 

  • Myers CM, Evans PD (1987) An FMRFamide antiserum differentiates between populations of antigens in the brain and retrocerebral complex of the locust,Schistocerca gregaria. Cell Tissue Res 250:93–99

    Google Scholar 

  • Nambu JR, Murphy-Erdosh C, Andrews PC, Feistner GJ, Scheller RH (1988) Isolation and characterization of aDrosophila neuropeptide family. Neuron 1:55–61

    PubMed  Google Scholar 

  • Nässel DR (1987) Aspects of the functional and chemical anatomy of the insect brain. In: Ali MA (ed) Nervous systems in invertebrates. Plenum, New York, pp 353–392

    Google Scholar 

  • Nässel DR, Ohlsson LG, Johansson KUI, Grimmelikhuijzen CJP (1988) Light and electron microscopic immunocytochemistry of neurons in the blowfly optic lobe reacting with antisera to RFamide and FMRFamide. Neuroscience 27:347–362

    PubMed  Google Scholar 

  • O'Donahue TL, Bishop JF, Chronwall BM, Groome J, Watson WH III (1984) Characterization and distribution of FMRFamide immunoreactivity in the rat central nervous system. Peptides 5:563–568

    PubMed  Google Scholar 

  • Painter SD, Greenberg MJ (1982) A survey of the responses of bivalve hearts to the molluscan neuropeptide FMRFamide and to 5-hydroxytryptamine. Biol Bull 162:311–332

    Google Scholar 

  • Price DA (1983) FMRFamide: assays and artifacts. In: Lever J, Boer HH (eds) Molluscan neuro-endocrinology. North Holland Publishing, Amsterdam, pp 184–189

    Google Scholar 

  • Price DA, Greenberg MJ (1977) Structure of a molluscan cardioexcitatory neuropeptide. Science 197:670–671

    PubMed  Google Scholar 

  • Price DA, Davies NW, Doble KE, Greenberg MJ (1987a) The variety and distribution of the FMRFamide-related peptides in molluscs. Zool Sci 4:395–410

    Google Scholar 

  • Price DA, Cobb CG, Doble KE, Kline JK, Greenberg MJ (1987b) Evidence for a novel FMRFamide-related heptapeptide in the pulmonate snailSiphonaria pectinata. Peptides 8:533–538

    PubMed  Google Scholar 

  • Raffa RB (1988) The action of FMRFamide (Phe-Met-Arg-Phe-NH2) and related peptides on mammals. Peptides 9:915–922

    PubMed  Google Scholar 

  • Rémy C, Guy J, Pelletier G, Boer HH (1988) Immunohistological demonstration of a substance related to neuropeptide Y and FMRFamide in the cephalic and thoracic nervous system of the locustSchistocerca gregaria. Cell Tissue Res 254:189–195

    PubMed  Google Scholar 

  • Robb S, Packman LC, Evans PD (1989) Isolation, primary structure and bioactivity of SchistoFLRFamide, a FMRFamide-like neuropeptide from the locust,Schistocerca gregaria. Biochem Biophys Res Commun 160:850–856

    PubMed  Google Scholar 

  • Schaefer M, Picciotto MR, Kreiner T, Kaldany RR, Taussig R, Scheller RH (1985)Aplysia neurons express a gene encoding FMRFamide neuropeptides. Cell 41:457–467

    PubMed  Google Scholar 

  • Schäfer S, Bicker G, Ottersen OP, Storm-Mathisen J (1988) Taurine-like immunoreactivity in the brain of the honeybee. J Comp Neurol 268:60–70

    PubMed  Google Scholar 

  • Schneider LE, Taghert PH (1988) Isolation and characterization of aDrosophila gene that encodes multiple neuropeptides related to Phe-Met-Arg-Phe-NH2 (FMRFamide). Proc Natl Acad Sci USA 85:1993–1997

    PubMed  Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry. Wiley, New York

    Google Scholar 

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

    Google Scholar 

  • Strausfeld NJ, Bacon JP (1983) Multimodal convergence in the central nervous system of dipterous insects. Fortschr Zool 28:47–76

    Google Scholar 

  • Takeda S, Viellemaringe J, Geffard M, Rémy C (1986) Immunohistological evidence of dopamine cells in the cephalic nervous system of the silkwormBombyx mori. Coexistence of dopamine and α endorphin-like substance in neurosecretory cells of the suboesophageal ganglion. Cell Tissue Res 243:125–128

    Google Scholar 

  • Taussig R, Scheller RH (1986) TheAplysia FMRFamide gene encodes sequences related to mammalian brain peptides. DNA 5:453–461

    PubMed  Google Scholar 

  • Taussig R, Scheller RH (1987) Modulation of ionic currents in the identified motoneuron B15 ofAplysia by 5-HT, SCPB, and FMRFamide. Soc Neurosci Abstr 13:40

    Google Scholar 

  • Trimmer BA, Kobierski LA, Kravitz EA (1987) Purification and characterization of FMRFamidelike immunoreactive substances from the lobster nervous system: Isolation and sequence analysis of two closely related peptides. J Comp Neurol 266:16–28

    PubMed  Google Scholar 

  • Veenstra JA (1987) Diversity in neurohemal organs for homologous neurosecretory cells in different insect species as demonstrated by immunocytochemistry with an antiserum to molluscan cardioexcitatory peptide. Neurosci Lett 73:33–37

    PubMed  Google Scholar 

  • Veenstra JA, Schooneveld H (1984) Immunocytochemical localization of neurons in the nervous system of the Colorado potato beetle with antisera against FMRFamide and bovine pancreatic polypeptide. Cell Tissue Res 235:303–308

    PubMed  Google Scholar 

  • Verhaert P, Grimmelikhuijzen CJP, DeLoof A (1985) Distinct localization of FMRFamide- and bovine pancreatic polypeptidelike material in the brain retrocerebral complex and suboesophageal ganglion in the cockroach,Periplaneta americana L. Brain Res 348:331–338

    PubMed  Google Scholar 

  • Walter C, Schäfer S (1988) FMRFamide-like immunoreactivity in the metathoracic ganglion of the locust (Schistocerca gregaria). Cell Tissue Res 253:489–491

    PubMed  Google Scholar 

  • Walter C, Schiebe M (1987) FMRF-NH2-like factor from neurohemal organ modulates neuromuscular transmission in the locust. Neurosci Lett 77:209–214

    PubMed  Google Scholar 

  • Walter C, Schiebe M, Voigt KH (1984) Synaptic and non-synaptic effects of cardioexcitatory neuropeptides on locust skeletal muscle. Neurosci Lett 45:99–104

    PubMed  Google Scholar 

  • Watson WH III, Groome JR, Chronwall BM, Bishop J, O'Donahue TL (1984) Presence and distribution of immunoreactive and bioactive FMRFamide-like peptides in the nervous system of the horseshoe crab,Limulus polyphemus. Peptides 5:585–592

    PubMed  Google Scholar 

  • White K, Hurteau T, Punsal P (1986) Neuropeptide-FMRFamidelike immunoreactivity inDrosophila: Development and distribution. J Comp Neurol 247:430–438

    PubMed  Google Scholar 

  • Williams JLD (1975) Anatomical studies of the insect central nervous system: A ground-plan of the midbrain and an introduction to the central complex in the locust,Schistocerca gregaria (Orthoptera). J Zool (Lond) 167:67–86

    Google Scholar 

  • Williams RG, Dockray GJ (1983) Immunohistochemical studies of FMRFamide-like immunoreactivity in rat brain. Brain Res 276:213–229

    PubMed  Google Scholar 

  • Yang H-YT, Fratta W, Majane EA, Costa E (1985) Isolation, sequencing, synthesis, and pharmacological characterization of two brain peptides that modulate the action of morphine. Proc Natl Acad Sci USA 82:7757–7761

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Homberg, U., Kingan, T.G. & Hildebrand, J.G. Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx mothManduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity. Cell Tissue Res. 259, 401–419 (1990). https://doi.org/10.1007/BF01740767

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01740767

Key words

Navigation