Abstract
Olfaction is an important sensory modality that regulates a plethora of behavioural expressions in insects. Processing of olfactory information takes place in the primary olfactory centres of the brain, namely the antennal lobes (ALs). Neuropeptides have been shown to be present in the olfactory system of various insect species. In the present study, we analyse the distribution of tachykinin, FMRFamide-related peptides, allatotropin, allatostatin, myoinhibitory peptides and SIFamide in the AL of the male Egyptian cotton leafworm, Spodoptera littoralis. Immunocytochemical analyses revealed that most neuropeptides were expressed in different subpopulations of AL neurons. Their arborisation patterns within the AL suggest a significant role of neuropeptide signalling in the modulation of AL processing. In addition to local interneurons, our analysis also revealed a diversity of extrinsic peptidergic neurons that connected the antennal lobe with other brain centres. Their distributions suggest that extrinsic neurons perform various types of context-related modulation.
Similar content being viewed by others
References
Anton S, Hansson BS (1994) Central processing of sex-pheromone, host odor, and oviposition deterrent information by interneurons in the antennal lobe of female Spodoptera littoralis (Lepidoptera, Noctuidae). J Comp Neurol 350:199–214
Anton S, Hansson BS (1995) Sex-pheromone and plant-associated odor processing in antennal lobe interneurons of male Spodoptera littoralis (lepidoptera, noctuidae). J Comp Physiol A 176:773–789
Barrozo RB, Gadenne C, Anton S (2010a) Switching attraction to inhibition: mating-induced reversed role of sex pheromone in an insect. J Exp Biol 213:2933–2939
Barrozo RB, Jarriault D, Simeone X, Gaertner C, Gadenne C, Anton S (2010b) Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin. J Exp Biol 213:1100–1106
Barrozo RB, Jarriault D, Deisig N, Gemeno C, Monsempes C, Lucas P, Gadenne C, Anton S (2011) Mating-induced differential coding of plant odour and sex pheromone in a male moth. Eur J Neurosci 33:1841–1850
Berg BG, Schachtner J, Utz S, Homberg U (2007) Distribution of neuropeptides in the primary olfactory center of the heliothine moth Heliothis virescens. Cell Tissue Res 327:385–398
Berg BG, Schachtner J, Homberg U (2009) Gamma-aminobutyric acid immunostaining in the antennal lobe of the moth Heliothis virescens and its colocalization with neuropeptides. Cell Tissue Res 335:593–605
Carlsson MA, Galizia CG, Hansson BS (2002) Spatial representation of odours in the antennal lobe of the moth Spodoptera littoralis (Lepidoptera: Noctuidae). Chem Senses 27:231–244
Carlsson MA, Diesner M, Schachtner J, Nässel DR (2010) Multiple neuropeptides in the Drosophila antennal lobe suggest complex modulatory circuits. J Comp Neurol 518:3359–3380
Dacks AM, Christensen TA, Hildebrand JG (2008) Modulation of olfactory information processing in the antennal lobe of Manduca sexta by serotonin. J Neurophysiol 99:2077–2085
Duve H, Thorpe A (2003) Neuropeptide co-localisation in the lepidopteran frontal ganglion studied by confocal laser scanning microscopy. Cell Tissue Res 311:79–89
Gadenne C, Dufour MC, Anton S (2001) Transient post-mating inhibition of behavioural and central nervous responses to sex pheromone in an insect. Proc R Soc Lond [Biol] 268:1631–1635
Heuer CM, Kollmann M, Binzer M, Schachtner J (2012) Neuropeptides in insect mushroom bodies. Arthropod Struct Dev 41:199–226
Hinks CF, Byers JR (1976) Biosystematics of genus Euxoa (Lepidoptera, Noctuidae). 5. Rearing procedures, and life-cycles of 36 species. Can Entomol 108:1345–1357
Homberg U, Müller U (1999) Neuroactive substances in the antennal lobe. In: Hansson BS (ed) Insect olfaction. Springer, Berlin, pp 181–206
Homberg U, Kingan TG, Hildebrand JG (1990) Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx moth Manduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity. Cell Tissue Res 259:401–419
Homberg U, Brandl C, Clynen E, Schoofs L, Veenstra JA (2004) Mas-allatotropin/Lom-AG-myotropin I immunostaining in the brain of the locust, Schistocerca gregaria. Cell Tissue Res 318:439–457
Ignell R (2001) Monoamines and neuropeptides in antennal lobe interneurons of the desert locust, Schistocerca gregaria: an immunocytochemical study. Cell Tissue Res 306:143–156
Ignell R, Root CM, Birse RT, Wang JW, Nässel DR, Winther AME (2009) Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc Natl Acad Sci USA 106:13070–13075
Iwano M, Kanzaki R (2005) Immunocytochemical identification of neuroactive substances in the antennal lobe of the male silkworm moth Bombyx mori. Zool Sci 22:199–211
Kim MY, Lee BH, Kwon D, Kang H, Nässel DR (1998) Distribution of tachykinin-related neuropeptide in the developing central nervous system of the moth Spodoptera litura. Cell Tissue Res 294:351–365
Lundquist CT, Brodin E, Muren JE, Nässel DR (1993) Tachykinin- and leucokinin-related peptides in the nervous system of the blowfly: immunocytochemical and chromatographical diversity. Peptides 14:651–663
Nässel DR (1993) Neuropeptides in the insect brain: a review. Cell Tissue Res 273:1–29
Nässel DR (1999) Tachykinin-related peptides in invertebrates: a review. Peptides 20:141–158
Nässel DR, Homberg U (2006) Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326:1–24
Nässel DR, Winther AM (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42–104
Nässel DR, Enell LE, Santos JG, Wegener C, Johard HA (2008) A large population of diverse neurons in the Drosophila central nervous system expresses short neuropeptide F, suggesting multiple distributed peptide functions. BMC Neurosci 9:90
Neupert S, Fusca D, Schachtner J, Kloppenburg P, Predel R (2012) Toward a single-cell-based analysis of neuropeptide expression in Periplaneta americana antennal lobe neurons. J Comp Neurol 520:694–716
Nichols R (2003) Signaling pathways and physiological functions of Drosophila melanogaster FMRFamide-related peptides. Annu Rev Entomol 48:485–503
Ochieng SA, Anderson P, Hansson BS (1995) Antennal lobe projection patterns of olfactory receptor neurons involved in sex pheromone detection in Spodoptera littoralis (Lepidoptera: Noctuidae). Tissue Cell 27:221–232
Orchard I, Lange AB, Bendena WG (2001) FMRFamide-related peptides: a multifunctional family of structurally related neuropeptides in insects. Adv Insect Physiol 28:267–329
Predel R, Rapus J, Eckert M (2001) Myoinhibitory neuropeptides in the American cockroach. Peptides 22:199–208
Rodriguez J, Deinhardt F (1960) Preparation of a semipermanent mounting medium for fluorescent antibody studies. Virology 12:316–317
Root CM, Ko KI, Jafari A, Wang JW (2011) Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell 145:133–144
Salio C, Lossi L, Ferrini F, Merighi A (2006) Neuropeptides as synaptic transmitters. Cell Tissue Res 326:583–598
Saveer AM, Kromann SH, Birgersson G, Bengtsson M, Lindblom T, Balkenius A, Hansson BS, Witzgall P, Becher PG, Ignell R (2012) Floral to green: mating switches moth olfactory coding and preference. Proc R Soc Lond [Biol] 279:2314–2322
Schachtner J, Trosowski B, D'Hanis W, Stubner S, Homberg U (2004) Development and steroid regulation of RFamide inummoreactivity in antennal-lobe neurons of the sphinx moth Manduca sexta. J Exp Biol 207:2389–2400
Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea plus Hexapoda). Arthropod Struct Dev 34:257–299
Schafer S, Rehder V (1989) Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 280:43–58
Sinakevitch I, Sjöholm M, Hansson BS, Strausfeld NJ (2008) Global and local modulatory supply to the mushroom bodies of the moth Spodoptera littoralis. Arthropod Struct Dev 37:260–272
Sjöholm M, Sinakevitch I, Strausfeld NJ, Ignell R, Hansson BS (2006) Functional division of intrinsic neurons in the mushroom bodies of male Spodoptera littoralis revealed by antibodies against aspartate, taurine, FMRF-amide, Mas-allatotropin and DC0. Arthropod Struct Dev 35:153–168
Terhzaz S, Rosay P, Goodwin SF, Veenstra JA (2007) The neuropeptide SIFamide modulates sexual behavior in Drosophila. Biochem Biophys Res Commun 352:305–310
Utz S, Schachtner J (2005) Development of A-type allatostatin immunoreactivity in antennal lobe neurons of the sphinx moth Manduca sexta. Cell Tissue Res 320:149–162
Utz S, Huetteroth W, Wegener C, Kahnt J, Predel R, Schachtner J (2007) Direct peptide profiling of lateral cell groups of the antennal lobes of Manduca sexta reveals specific composition and changes in neuropeptide expression during development. Dev Neurobiol 67:764–777
Veenstra JA, Hagedorn HH (1993) Sensitive enzyme-immunoassay for Manduca allatotropin and the existence of an allatotropin-immunoreactive peptide in Periplaneta americana. Arch Insect Biochem 23:99–109
Winther AME, Ignell R (2010) Local peptidergic signaling in the antennal lobe shapes olfactory behavior. Fly 4:167–171
Winther AM, Nässel DR (2001) Intestinal peptides as circulating hormones: release of tachykinin-related peptide from the locust and cockroach midgut. J Exp Biol 204:1269–1280
Winther AM, Muren JE, Ahlborg N, Nässel DR (1999) Differential distribution of isoforms of Leucophaea tachykinin-related peptides (LemTRPs) in endocrine cells and neuronal processes of the cockroach midgut. J Comp Neurol 406:15–28
Winther AME, Acebes A, Ferrus A (2006) Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol Cell Neurosci 31:399–406
Acknowledgments
We thank Dr. Dick Nässel, Dr. Jan Veenstra, Dr. Allan Thorpe and Dr. Reinhard Predel for kindly supplying the various antisera. We are also grateful to Elisabeth Marling (Swedish University of Agricultural Sciences, Sweden) for the rearing of the insects.
Author information
Authors and Affiliations
Corresponding author
Additional information
This study was supported by the Swedish Research Council, Formas and the Linnaeus-programme Insect Chemical Ecology, Ethology and Evolution, IC-E3.
Rights and permissions
About this article
Cite this article
Kromann, S.H., Hansson, B.S. & Ignell, R. Distribution of neuropeptides in the antennal lobes of male Spodoptera littoralis . Cell Tissue Res 354, 431–440 (2013). https://doi.org/10.1007/s00441-013-1703-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-013-1703-x