Skip to main content
Log in

Regeneration of axotomized olfactory neurons in young and adult locusts quantified by fasciclin I immunofluorescence

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

Abstract

The olfactory pathway of the locust Locusta migratoria is characterized by a multiglomerular innervation of the antennal lobe (AL) by olfactory receptor neurons (ORNs). After crushing the antenna and thereby severing ORN axons, changes in the AL were monitored. First, volume changes were measured at different times post-crush with scanning laser optical tomography in 5th instar nymphs. AL volume decreased significantly to a minimum volume at 4 days post-crush, followed by an increase. Second, anterograde labeling was used to visualize details in the AL and antennal nerve (AN) during de- and regeneration. Within 24 h post-crush (hpc) the ORN fragments distal to the lesion degenerated. After 48 hpc, regenerating fibers grew through the crush site. In the AL, labeled ORN projections disappeared completely and reappeared after a few days. A weak topographic match between ORN origin on the antenna and the position of innervated glomeruli that was present in untreated controls did not reappear after regeneration. Third, the cell surface marker fasciclin I that is expressed in ORNs was used for quantifying purposes. Immunofluorescence was measured in the AL during de- and regeneration in adults and 5th instar nymphs: after a rapid but transient, decrease, it reappeared. Both processes happen faster in 5th instar nymphs than in adults.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Anton S, Hansson BS (1996) Antennal lobe interneurons in the desert locust Schistocerca gregaria (Forskal): Processing of aggregation pheromones in adult males and females. J Comp Neurol 370:85–96

    Article  CAS  PubMed  Google Scholar 

  • Anton S, Ignell R, Hansson BS (2002) Developmental changes in the structure and function of the central olfactory system in gregarious and solitary desert locusts. Microsc Res Tech 56:281–291. doi:10.1002/jemt.10032

    Article  PubMed  Google Scholar 

  • Ayaz D, Leyssen M, Koch M, Yan J, Srahna M, Sheeba V, Fogle KJ, Holmes TC, Hassan BA (2008) Axonal injury and regeneration in the adult brain of Drosophila. J Neurosci 28:6010–6021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bastiani MJ, Harrelson AL, Snow PM, Goodman CS (1987) Expression of fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grasshopper. Cell 48:745–755

    Article  CAS  PubMed  Google Scholar 

  • Bittner GD (1991) Long-term survival of anucleate axons and its implication for nerve regeneration. Trends Neurosci 14:188–193

    Article  CAS  PubMed  Google Scholar 

  • Blackmore M, Letourneau PC (2006) Changes within maturing neurons limit axonal regeneration in the developing spinal cord. J Neurobiol 66:348–360

    Article  CAS  PubMed  Google Scholar 

  • Boeckh J, Tolbert LP (1993) Synaptic organization and development of the antennal lobe in insects. Microsc Res Tech 24:260–280. doi:10.1002/jemt.1070240305

    Article  CAS  PubMed  Google Scholar 

  • Carbonetto S, Muller KJ (1972) A regenerating neurone in the leech can form an electrical synapse on its severed axon segment. Nature 267:450–451

    Article  Google Scholar 

  • Chapman RF, Greenwood M (1984) Differences in numbers of sensilla on the antennae of solitarious and gregarious Locusta migratoria L. (Orthoptera: Acrididae). Int J Insect Morphol Embryol 13:295–301

    Article  Google Scholar 

  • Chapman RF, Greenwood M (1986) Changes in distribution and abundance of antennal sensilla during growth of Locusta migratoria L. (Orthoptera : Acrididae). Int J Insect Morphol Embryol 15:83–96

    Article  Google Scholar 

  • Chiba A, Murphey RK (1991) Connectivity of identified central synapses in the cricket is normal following regeneration and blockade of presynaptic activity. J Neurobiol 22:130–142

    Article  CAS  PubMed  Google Scholar 

  • Eickhoff R, Bicker G (2012) Developmental expression of cell recognition molecules in the mushroom body and antennal lobe of the locust Locusta migratoria. J Comp Neurol 520:2021–2040

    Article  CAS  PubMed  Google Scholar 

  • Eickhoff R, Lorbeer RA, Scheiblich H, Heisterkamp A, Meyer H, Stern M, Bicker G (2012) Scanning laser optical tomography resolves structural plasticity during regeneration in an insect brain. PLoS ONE 7, e41236. doi:10.1371/journal.pone.0041236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ernst KD, Boeckh J, Boeckh V (1977) A neuroanatomical study on the organization of the central antennal pathways in insects. Z Zellforsch 176:285–306

    CAS  Google Scholar 

  • Fredman SM, Nutz PG (1988) Regeneration of identified neurons and their synaptic connections in the central nervous system of Aplysia. Am Zool 28:1099–1108

    Article  Google Scholar 

  • Galizia CG, Rössler W (2010) Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55:399–420

    Article  CAS  PubMed  Google Scholar 

  • Gewecke M (1972) Bewegungsmechanismus und Gelenkrezeptoren der Antennen von Locusta migratoria L. (Insecta, Orthoptera). Z Morph Tiere 71:128–149

    Article  Google Scholar 

  • Ghannad-Rezaie M, Wang X, Mishra B, Collins C, Chronis N (2012) Microfluidic chips for in vivo imaging of cellular responses to neural injury in Drosophila larvae. PLoS ONE 7(1), e29869. doi:10.1371/journal.pone.0029869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guthrie DM (1962) Regenerative growth in insect nerve axons. Insect Physiol 8:79–92

    Article  Google Scholar 

  • Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72:698–711. doi:10.1016/j.neuron.2011.11.003

    Article  CAS  PubMed  Google Scholar 

  • Huetteroth W, Schachtner J (2005) Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study both developmental and adult neuronal plasticity. Cell Tissue Res 319:513–524

    Article  PubMed  Google Scholar 

  • Ignell R, Anton S, Hansson BS (2001) The antennal lobe of Orthoptera - anatomy and evolution. Brain Behav Evol 57:1–17

    Article  CAS  PubMed  Google Scholar 

  • Jacobs K, Lakes-Harlan R (1999) Axonal degeneration with tympanal nerve of Schistocerca gregaria. Cell Tissue Res 298:167–178

    Article  CAS  PubMed  Google Scholar 

  • Jefferis GS, Hummel T (2006) Wiring specificity in the olfactory system. Semin Cell Dev Biol 17:50–65

    Article  PubMed  Google Scholar 

  • Kirchhof B, Bicker G (1992) Growth properties of larval and adult locust neurons in primary cell culture. J Comp Neurol 323:411–422

    Article  CAS  PubMed  Google Scholar 

  • Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154–3165

    CAS  PubMed  Google Scholar 

  • Komiyama T, Sweeney LB, Schuldiner O, Garcia KC, Luo L (2007) Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128:399–410

  • Kraft R, Levine RB, Restifo LL (1998) The Steroid Hormone 20-Hydroxyecdysone Enhances Neurite Growth of Drosophila Mushroom Body Neurons Isolated during Metamorphosis. J Neurosci 18:8886–8899

    CAS  PubMed  Google Scholar 

  • Krüger S, Butler CS, Lakes-Harlan R (2011a) Morphological and physiological regeneration in the auditory system of adult Mecopoda elongata (Orthoptera: Tettigoniidae). J Comp Physiol A 197:181–192

    Article  Google Scholar 

  • Krüger S, Haller B, Lakes-Harlan R (2011b) Regeneration in the auditory system of nymphal and adult bush crickets Tettigonia viridissima. Physiol Entomol 36:235–246

    Article  Google Scholar 

  • Krüger S, Lakes-Harlan R (2010) Changes in the auditory neuropil after deafferentation in adult grasshoppers (Schistocerca gregaria). Arthropod Struct Dev 39:26–32

    Article  PubMed  Google Scholar 

  • Lakes R, Kalmring K, Engelhardt KH (1990) Changes in the auditory system of locusts (Locusta migratoria and Schistocerca gregaria) after deafferentation. J Comp Physiol A 166:553–563

    Article  Google Scholar 

  • Lapper SR, Bolam JP (1991) The anterograde and retrograde transport of neurobiotin in the central nervous system of the rat: comparison with biocytin. J Neurosci Methods 39:163–174

    Article  CAS  PubMed  Google Scholar 

  • Laurent G (1996) Dynamical representation of odors by oscillating and evolving neural assemblies. Trends Neurosci 19:489–496

    Article  CAS  PubMed  Google Scholar 

  • Lorbeer RA, Heidrich M, Lorbeer C, Ramirez Ojeda DF, Bicker G, Meyer H, Heisterkamp A (2011) Highly efficient 3D fluorescence microscopy with a scanning laser optical tomograph. Opt Express 19:5419–5430

    Article  CAS  PubMed  Google Scholar 

  • Newland PL (1991) Morphology and somatotopic organisation of the central projections of afferents from tactile hairs on the hind leg of the locust. J Comp Neurol 312:493–508

    Article  CAS  PubMed  Google Scholar 

  • Newland PL, Rogers SM, Gaaboub I, Matheson T (2000) Parallel somatotopic maps of gustatory and mechanosensory neurons in the central nervous system of an insect. J Comp Neurol 425:82–96

    Article  CAS  PubMed  Google Scholar 

  • Ostrowski D, Ehrenreich H, Heinrich R (2011) Erythropoietin promotes survival and regeneration of insect neurons in vivo and in vitro. Neuroscience 188:95–108

    Article  CAS  PubMed  Google Scholar 

  • Ott SR (2008) Confocal microscopy in large insect brains: zinc-formaldehyde fixation improves synapsin immunostaining and preservation of morphology in whole-mounts. J Neurosci Methods 172:220–230. doi:10.1016/j.jneumeth.2008.04.031

    Article  CAS  PubMed  Google Scholar 

  • Pätschke A, Bicker G, Stern M (2004) Axonal regeneration of proctolinergic neurons in the central nervous system of the locust. Brain Res Dev Brain Res 150:73–76

    Article  PubMed  Google Scholar 

  • Rossignol S, Schwab M, Schwartz M, Fehlings MG (2007) Spinal cord injury: time to move? J Neurosci 27:11782–11792

    Article  CAS  PubMed  Google Scholar 

  • Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea þ Hexapoda). Arthropod Struct Dev 34:257–299

    Article  Google Scholar 

  • Schneider D (1964) Insect antennae. Annu Rev Entomol 9:103–122

    Article  Google Scholar 

  • Schürmann FW, Wechsler W (1970) Synapsen im Antennenhügel von Locusta migratoria (Orthoptera, Insecta). Z Zellforsch 108:563–581

    Article  PubMed  Google Scholar 

  • Simões P, Ott SR, Niven JE (2011) Associative olfactory learning in the desert locust. Schistocerca gregaria. J Exp Biol 214:2495–2503. doi:10.1242/jeb.055806

    Article  PubMed  Google Scholar 

  • Spira ME, Zeldes D, Hochner B, Dormann A (1987) The effects of microenvironment on the redifferentiation of regenerating neurones: neurite architecture, acetylcholine receptors and Ca2+ channel distribution. J Exp Biol 132:111–131

    CAS  PubMed  Google Scholar 

  • Stern M, Bicker G (2008) Nitric oxide regulates axonal regeneration in an insect embryonic CNS. Dev Neurosci 68:295–308

    CAS  Google Scholar 

  • Stern M, Ediger VL, Gibbon CR, Blagburn JM, Bacon JP (1997) Regeneration of cercal filiform hair sensory neurons in the first-instar cockroach restores escape behaviour. J Neurobiol 33:439–458

    Article  CAS  PubMed  Google Scholar 

  • Stern M, Scheiblich H, Eickhoff R, Diwischus N, Bicker G (2012) Regeneration of olfactory afferent axons in the locust brain. J Comp Neurol 520:679–693

    Article  CAS  PubMed  Google Scholar 

  • Vosshall LB, Wong AM, Axel R (2000) An olfactory sensory map in the fly brain. Cell 102:147–159. doi:10.1016/S0092-8674(00)00021-0

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Yang P, Chen D, Jiang F, Li Y, Wang X, Kang L (2015) Identification and functional analysis of olfactory receptor family reveal unusual characteristics of the olfactory system in the migratory locust. Cell Mol Life Sci 72:4429–4443. doi:10.1007/s00018-015-2009-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waller A (1850) Experiments on the section of glossopharyngeal and hypoglossal nerves of the frog and observations of the alternatives produced thereby in the structure of their primitive fibres. Philos Trans R Soc Lond B 140:423–429

    Article  Google Scholar 

  • Xiong X, Wang X, Ewanek R, Bhat P, DiAntonio A, Collins CA (2010) Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury. J Cell Biol 191:211–223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zwart MF, Randlett O, Evers JF, Landgraf M (2013) Dendritic growth gated by a steroid hormone receptor underlies increases in activity in the developing Drosophila locomotor system. Proc Natl Acad Sci U S A 110:E3878–E3887. doi:10.1073/pnas.1311711110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The study was partially funded by the German Federal Ministry for Education and Research (BMBF grant 031L0062A).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Stern.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wasser, H., Biller, A., Antonopoulos, G. et al. Regeneration of axotomized olfactory neurons in young and adult locusts quantified by fasciclin I immunofluorescence. Cell Tissue Res 368, 1–12 (2017). https://doi.org/10.1007/s00441-016-2560-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-016-2560-1

Keywords

Navigation