Skip to main content
Log in

Standardized atlas of the brain of the desert locust, Schistocerca gregaria

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

Abstract

In order to understand the connectivity of neuronal networks, their constituent neurons should ideally be studied in a common framework. Since morphological data from physiologically characterized and stained neurons usually arise from different individual brains, this can only be performed in a virtual standardized brain that compensates for interindividual variability. The desert locust, Schistocerca gregaria, is an insect species used widely for the analysis of olfactory and visual signal processing, endocrine functions, and neural networks controlling motor output. To provide a common multi-user platform for neural circuit analysis in the brain of this species, we have generated a standardized three-dimensional brain of this locust. Serial confocal images from whole-mount locust brains were used to reconstruct 34 neuropil areas in ten brains. For standardization, we compared two different methods: an iterative shape-averaging (ISA) procedure by using affine transformations followed by iterative nonrigid registrations, and the Virtual Insect Brain (VIB) protocol by using global and local rigid transformations followed by local nonrigid transformations. Both methods generated a standard brain, but for different applications. Whereas the VIB technique was designed to visualize anatomical variability between the input brains, the purpose of the ISA method was the opposite, i.e., to remove this variability. A novel individually labeled neuron, connecting the lobula to the midbrain and deutocerebrum, has been registered into the ISA atlas and demonstrates its usefulness and accuracy for future analysis of neural networks. The locust standard brain is accessible at http://www.3d-insectbrain.com.

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
Fig. 10
Fig. 11

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  PubMed  CAS  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

    Article  PubMed  Google Scholar 

  • Berg BG, Galizia CG, Brandt R, Mustaparta H (2002) Digital atlases of the antennal lobe in two species of tobacco budworm moths, the oriental Helicoverpa assulta (male) and the american Heliothis virescens (male and female). J Comp Neurol 446:123–134

    Article  PubMed  Google Scholar 

  • Boyan G, Reichert H, Hirth F (2003) Commissure formation in the embryonic insect brain. Arthropod Struct Dev 32:61–77

    Article  PubMed  Google Scholar 

  • Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Hege HC, Menzel R (2005) Three-dimensional average-shape atlas of the honeybee brain and its applications. J Comp Neurol 492:1–19

    Article  PubMed  Google Scholar 

  • Bucher D, Scholz M, Stetter M, Obermayer K, Pflüger HJ (2000) Correction methods for three-dimensional reconstructions from confocal images. I. Tissue shrinking and axial scaling. J Neurosci Methods 100:135–143

    Article  PubMed  CAS  Google Scholar 

  • Burrows M (1996) The neurobiology of an insect brain. Oxford University Press, Oxford

    Google Scholar 

  • Cassenaer S, Laurent G (2007) Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448:709–714

    Article  PubMed  CAS  Google Scholar 

  • Chiang AS, Liu YC, Chiu SL, Hu SH, Huang CY, Hsieh CH (2001) Three-dimensional mapping of brain neuropils in the cockroach, Diploptera punctata. J Comp Neurol 440:1–11

    Article  PubMed  CAS  Google Scholar 

  • Clements AN, May TE (1974) Studies on locust neuromuscular physiology in relation to glutamic acid. J Exp Biol 60:673–705

    PubMed  CAS  Google Scholar 

  • Crum WR, Camara O, Rueckert D, Bhatia KK, Jenkinson M, Hill DL (2005) Generalised overlap measures for assessment of pairwise and groupwise image registration and segmentation. In: Duncan JS, Gerig G (eds) Medical image computing and computer-assisted intervention, MICCAI 8th International Conference, Palm Springs, Calif., USA. Proceedings, Part I, vol 3749 of Lecture Notes in Computer Science. Springer, Berlin Heidelberg New York, pp 99–106

    Google Scholar 

  • Davis RL (1993) Mushroom bodies and Drosophila learning. Neuron 11:1–14

    Article  PubMed  CAS  Google Scholar 

  • Elphick MR, Williams L, O’Shea M (1996) New features of the locust optic lobe: evidence of a role for nitric oxide in insect vision. J Exp Biol 199:2395–2407

    PubMed  CAS  Google Scholar 

  • Erber J, Schildberger K (1980) Conditioning of an antennal reflex to visual stimuli in bees (Apis mellifera L.). J Comp Physiol 135:217–225

    Article  Google Scholar 

  • Erber J, Pribbenow B, Grandy K, Kierzek S (1997) Tactile motor learning in the antennal system of the honeybee (Apis mellifera L.). J Comp Physiol [A] 181:355–365

    Article  Google Scholar 

  • Evers JF, Schmitt S, Sibila M, Duch C (2005) Progress in functional neuroanatomy: precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. J Neurophysiol 93:2331–2342

    Article  PubMed  CAS  Google Scholar 

  • Farris SM, Robinson GE, Fahrbach SE (2001) Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J Neurosci 21:6395–6404

    PubMed  CAS  Google Scholar 

  • Galizia CG, Mellwrath SL, Menzel R (1999) A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383–394

    Article  PubMed  CAS  Google Scholar 

  • Gewecke M, Hou T (1992) Structure and function of visual interneurons in the locust brain. In: Singh RN (ed) Nervous systems, principles of design and function. Wiley, New Delhi, pp 255–270

    Google Scholar 

  • Gewecke M, Hou T (1993) Visual brain neurons in Locusta migratoria. In: Wiese K, Kapitsky S, Renninger G (eds) Sensory systems of arthropods. Birkhäuser, Basel, pp 119–144

    Google Scholar 

  • Gouranton J (1964) Contribution a l`étude de la structure des ganglions cérébröides de Locusta migratoria migratorioides. Bull Soc Zool France 89:785–797

    Google Scholar 

  • Greiner B, Gadenne C, Anton S (2004) Three-dimensional antennal lobe atlas of the male moth, Agrotis ipsilon: a tool to study structure-function correlation. J Comp Neurol 475:205–210

    Article  Google Scholar 

  • Heinze S, Homberg U (2007) Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315:995–997

    Article  PubMed  CAS  Google Scholar 

  • Heisenberg M (1998) What do the mushroom bodies do for the insect brain? Learn Mem 5:1–10

    PubMed  CAS  Google Scholar 

  • Homberg U (1994) Distribution of neurotransmitters in the insect brain. Progress in Zoology, vol 40. Fischer, Stuttgart

    Google Scholar 

  • Homberg U (2004) In search of the sky compass in the insect brain. Naturwissenschaften 91:199–208

    Article  PubMed  CAS  Google Scholar 

  • Homberg U, Hofer S, Pfeiffer K, Gebhardt S (2003) Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. J Comp Neurol 462:415–430

    Article  PubMed  Google Scholar 

  • Honegger HW (1981) A preliminary note of a new optomotor response in crickets: antennal tracking of moving targets. J Comp Physiol 142:419–421

    Article  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 

  • Iyengar BG, Chou CJ, Sharma A, Atwood HL (2006) Modular neuropile organization in the Drosophila larval brain facilitates identification and mapping of central neurons. J Comp Neurol 499:583–602

    Article  PubMed  Google Scholar 

  • Jefferis GSXE, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR Jr, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128:1187–1203

    Article  PubMed  CAS  Google Scholar 

  • Jenett A, Schindelin JE, Heisenberg M (2006) The Virtual Insect Brain protocol: creating and comparing standardized neuroanatomy. BMC Bioinformatics 7:544

    Article  PubMed  CAS  Google Scholar 

  • Jortner RA, Farivar SS, Laurent G (2007) A simple connectivity scheme for sparse coding in an olfactory system. J Neurosci 27:1659–1669

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita M, Pfeiffer K, Homberg U (2007) Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria. J Exp Biol 210:1350–1361

    Article  PubMed  Google Scholar 

  • Kwon H-W, Lent DD, Strausfeld NJ (2004) Spatial learning in the restrained American cockroach Periplaneta americana. J Exp Biol 207:377–383

    Article  PubMed  Google Scholar 

  • Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543–552

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nature Rev Neurosci 3:884–895

    Article  CAS  Google Scholar 

  • Liu G, Seiler H, Wen A, Zars T, Ito K, Wolf R, Heisenberg M, Liu L (2006) Distinct memory traces for two visual features in the Drosophila brain. Nature 439:551–556

    Article  PubMed  CAS  Google Scholar 

  • Lozano VC, Armengaud C, Gauthier M (2001) Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. J Comp Physiol [A] 187:249–254

    Article  CAS  Google Scholar 

  • Ludwig P, Williams L, Nässel DR, Reichert H, Boyan G (2001) Primary commissure pioneer neurons in the brain of the grasshopper Schistocerca gregaria: development, ultrastructure, and neuropeptide expression. J Comp Neurol 430:118–130

    Article  PubMed  CAS  Google Scholar 

  • Malun D, Plath N, Giurfa M, Moseleit AD, Müller U (2002) Hydroxyurea-induced partial mushroom body ablation in the honeybee Apis mellifera: volumetric analysis and quantitative protein determination. J Neurobiol 50:31–44

    Article  PubMed  CAS  Google Scholar 

  • Martone ME, Gupta A, Ellisman MH (2004) e-Neuroscience: challenges and triumphs in integrating distributed data from molecules to brains. Nat Neurosci 7:467–472

    Article  PubMed  CAS  Google Scholar 

  • Masante-Roca I, Gadenne C, Anton S (2005) Three-dimensional antennal lobe atlas of male and female moths, Lobesia botrana (Lepidoptera: Tortricidae) and glomerular representation of plant volatiles in females. J Exp Biol 208:1147–1159

    Article  PubMed  Google Scholar 

  • McGurk L, Morrison H, Keegan LP, Sharpe J, O’Connell MA (2007) Three-dimensional imaging of Drosophila melanogaster. PLoS ONE 2:e834

    Article  PubMed  CAS  Google Scholar 

  • Müller M, Homberg U, Kühn A (1997) Neuroarchitecture of the lower division of the central body in the brain of the locust (Schistocerca gregaria). Cell Tissue Res 288:159–176

    Article  PubMed  Google Scholar 

  • Müller U (1999) Second messenger pathways in the honeybee brain: immunohistochemistry of protein kinase A and protein kinase C. Microsc Res Tech 45:165–173

    Article  PubMed  Google Scholar 

  • Pfeiffer K, Homberg U (2007) Coding of azimuthal directions via time-compensated combination of celestial time cues. Curr Biol 17:960–965

    Article  PubMed  CAS  Google Scholar 

  • Pfeiffer K, Kinoshita M, Homberg U (2005) Polarization-sensitive and light-sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J Neurophysiol 94:3903–3915

    Article  PubMed  Google Scholar 

  • Rein K, Zöckler M, Mader MT, Grübel C, Heisenberg M (2002) The Drosophila standard brain. Curr Biol 12:227–231

    Article  PubMed  CAS  Google Scholar 

  • Reischig T, Stengl M (2002) Optic lobe commissures in a three-dimensional brain model of the cockroach Leucophaea maderae: a search for the circadian coupling pathways. J Comp Neurol 443:388–400

    Article  PubMed  Google Scholar 

  • Rind FC (1987) Non-directional, movement sensitive neurones of the locust optic lobe. J Comp Physiol [A] 161:477–494

    Article  Google Scholar 

  • Rind FC (2002) Motion detectors in the locust visual system: from biology to robot sensors. Microsc Res Tech 56:256–269

    Article  PubMed  Google Scholar 

  • Rohlfing T, Maurer CR Jr (2003) Nonrigid image registration in shared-memory multiprocessor environments with application to brains, breasts, and bees. IEEE Trans Inf Technol B 7:16–25

    Article  Google Scholar 

  • Rohlfing T, Brandt R, Maurer CR Jr, Menzel R (2001) Bee brains, B-splines and computational democracy: generating an average shape atlas. Proceedings of the IEEE Workshop on Mathematical Methods in Biomedical Image Analysis, MMBIA, Kauai, Hawaii, pp 187–194 (http://doi.ieeecomputersociety.org/10.1109/MMBIA.2001.991733)

  • Rø H, Müller D, Mustaparta H (2007) Anatomical organization of antennal lobe projection neurons in the moth Heliothis virescens. J Comp Neurol 500:658–675

    Article  PubMed  Google Scholar 

  • Rospars JP, Hildebrand JG (2000) Sexually dimorphic and isomorphic glomeruli in the antennal lobe of the sphinx moth Manduca sexta. Chem Senses 25:119–129

    Article  PubMed  CAS  Google Scholar 

  • Rueckert D, Sonoda LI, Hayes C, Hill DLG, Leach MO, Hawkes DJ (1999) Nonrigid registration using free-form deformations: application to breast MR images. IEEE Trans Med Imaging 18:712–721

    Article  PubMed  CAS  Google Scholar 

  • Rueckert D, Frangi AF, Schnabel JA (2003) Automatic construction of 3-D statistical deformation models of the brain using nonrigid registration. IEEE Trans Med Imaging 22:1014–1025

    Article  PubMed  Google Scholar 

  • Rybak J, Menzel R (1998) Integrative properties of the Pe1 neuron, a unique mushroom body output neuron. Learn Mem 5:133–145

    PubMed  CAS  Google Scholar 

  • Sadek MM, Hansson BS, Rospars JP, Anton S (2002) Glomerular representation of plant volatiles and sex pheromone components in the antennal lobe of the female Spodoptera littoralis. J Exp Biol 205:1363–1376

    PubMed  CAS  Google Scholar 

  • Schindelin J (2005) The standard brain of Drosophila melanogaster and its automatic segmentation. PhD thesis, University of Würzburg, Germany

  • Schmitt S, Evers JF, Duch C, Scholz M, Obermayer K (2004) New methods for the computer-assisted 3-D reconstruction of neurons from confocal image stacks. Neuroimage 23:1283–1298

    Article  PubMed  Google Scholar 

  • Simmons PJ (2002) Signal processing in a simple visual system: the locust ocellar system and its synapses. Microsc Res Tech 56:270–280

    Article  PubMed  Google Scholar 

  • Smid HM, Bleeker MAK, Loon JJA van, Vet LEM (2003) Three-dimensional organization of the glomeruli in the antennal lobe of the parasitoid wasps Cotesia glomerata and C. rubecula. Cell Tissue Res 312:237–248

    PubMed  Google Scholar 

  • Stern M, Gewecke M (1993) Spatial sensitivity profiles of motion sensitive neurons in the locust brain. In: Wiese K, Kapitsky S, Renninger G (eds) Sensory systems of arthropods. Birkhäuser, Basel, pp 184–195

    Google Scholar 

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

    Google Scholar 

  • Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633–638

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Toga AW (2002) Neuroimage databases: the good, the bad and the ugly. Nat Rev Neurosci 3:302–308

    Article  PubMed  CAS  Google Scholar 

  • Toga AW (2005) Computational biology for vizualization of brain structure. Anat Embryol 210:422–438

    Article  Google Scholar 

  • Toga AW, Thompson PM (2001) Maps of the brain. Anat Rec 265:37–53

    Article  PubMed  CAS  Google Scholar 

  • Van Essen DC (2002) Windows on the brain: the emerging role of atlases and databases in neuroscience. Curr Opin Neurobiol 12:574–579

    Article  PubMed  Google Scholar 

  • Veelaert D, Schoofs L, De Loof A (1998) Peptidergic control of the corpus cardiacum–corpora allata complex of locusts. Int Rev Cytol 182:249–302

    Article  PubMed  CAS  Google Scholar 

  • Wahba G (1990) Spline models for observational data. CBMS-NSF Regional Conference Series, vol 59. SIAM, Philadelphia

    Google Scholar 

  • Zöckler M, Rein K, Brandt R, Stalling D, Hege HC (2001) Creating virtual insect brains with Amira. ZIB Report 01-32:1–11

    Google Scholar 

Download references

Acknowledgements

We thank Dr. Erich Buchner (Universität Würzburg, Würzburg, Germany) for providing antibodies, Dr. Robert Brandt (Mercury Computer Systems, Berlin, Germany) for providing the AmiraZIB license and for help with Amira (especially concerning the use of the “Arithmetic” module), and Ulrike Träger for providing confocal images of the stained lobula projection neuron.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Uwe Homberg.

Additional information

This work was supported by the Deutsche Forschungsgemeinschaft (U. Homberg; HO 950/14-3) and the National Institute on Alcohol Abuse and Alcoholism (T. Rohlfing; AA05965 and AA13521).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kurylas, A.E., Rohlfing, T., Krofczik, S. et al. Standardized atlas of the brain of the desert locust, Schistocerca gregaria . Cell Tissue Res 333, 125–145 (2008). https://doi.org/10.1007/s00441-008-0620-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-008-0620-x

Keywords

Navigation