The locust standard brain: A 3D standard of the central complex as a platform for neural network analysis

Frontiers in Systems Neuroscience

Volumn 3, Issue FEB, 2010, Pages

  el Jundi, Basil ^a   Heinze, Stanley ^a,c   Lenschow, Constanze ^a,d   Kurylas, Angela ^a   Rohlfing, Torsten ^b   Homberg, Uwe ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b SRI INTERNATIONAL   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

3D; Central complex; Desert locust; Digital neuroanatomy; Iterative shape averaging; Single cell registration; Standard brain; Virtual insect brain

Indexed keywords

EID: 84885976968     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.06.021.2009     Document Type: Article

References (51)

1. Blum, M., and Labhart, T. (2000). Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye. J. Comp. Physiol. A 186, 119-128.
2. Brandt, R., Rohlfing, T., Rybak, J., Krofczik, S., Maye, A., Westerhoff, M., Hege, H. C., and Menzel, R. (2005). Threedimensional average-shape atlas of the honeybee brain and its applications. J. Comp. Neurol. 492, 1-19.
3. Bucher, D., Scholz, M., Stetter, M., Obermayer, K., and Pflüger, H. J. (2000). Correction methods for threedimensional reconstructions from confocal images: I. Tissue shrinking and axial scaling. J. Neurosci. Methods 100, 135-143.
4. el Jundi, B., Huetteroth, W., Kurylas, A. E., and Schachtner, J. (2009). Anisometric brain dimorphism revisited: implementation of a volumetric 3D standard brain in Manduca sexta. J. Comp. Neurol. 517, 210-225.
5. Evers, J. F., Schmitt, S., Sibila, M., and Duch, C. (2005). Progress in functional neuroanatomy: precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. J. Neurophysiol. 93, 2331-2342.
6. Hanesch, U., Fischbach, K. F., and Heisenberg, M. (1989). Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res. 257, 343-366.
7. Heinze, S. (2009). Characterization of Polarization Sensitive Neurons of the Central Complex in the Brain of the Desert Locust (Schistocerca gregaria). PhD Thesis, Philipps University Marburg, Marburg.
8. Heinze, S., Gotthardt, S., and Homberg, U. (2009). Transformation of polarized light information in the central complex of the locust. J. Neurosci. 29, 11783-11793.
9. Heinze, S., and Homberg, U. (2007). Maplike representation of celestial E-vector orientations in the brain of an insect. Science 315, 995-997.
10. Heinze, S., and Homberg, U. (2008). Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J. Comp. Neurol. 511, 454-478.
11. Heinze, S., and Homberg, U. (2009). Linking the input to the output: new sets of neurons complement the polarization vision network in the locust central complex. J. Neurosci. 29, 4911-4921.
12. Homberg, U. (1991). Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J. Comp. Neurol. 303, 245-254.
13. Homberg, U. (1994). Flight-correlated activity changes in neurons of the lateral accessory lobes in the brain of the locust Schistocerca gregaria. J. Comp. Physiol. A 175, 597-610.
14. Homberg, U. (2004). In search of the sky compass in the insect brain. Naturwissenschaften 91, 199-208.
15. Homberg, U., Hofer, S., Pfeiffer, K., and 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.
16. Homberg, U., and Paech, A. (2002). Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct. Dev. 30, 271-280.
17. Homberg, U., Vitzthum, H., Müller, M., and Binkle, U. (1999). Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides. J. Comp. Neurol. 409, 495-507.
18. Horváth, G., and Varjú, D. (2004). Polarization Patterns in Nature and Polarized Light in Animal Vision. Berlin, Heidelberg, New York, Springer Verlag.
19. Ilius, M., Wolf, R., and Heisenberg, M. (1994). The central complex of Drosophila melanogaster is involved in fl ight control: studies on mutants and mosaics of the gene ellipsoid body open. J. Neurogenet. 9, 189-206.
20. Jenett, A., Schindelin, J. E., and Heisenberg, M. (2006). The virtual insect brain protocol: creating and comparing standardized neuroanatomy. BMC Bioinformatics 7, 544.
21. Kinoshita, M., Pfeiffer, K., and 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.
22. Klagges, B. R. E., Heimbeck, G., Godenschwege, T. A., Hofbauer, A., Pflugfelder, G. O., Reifegerste, R., Reisch, D., Schaupp, M., Buchner, S., and Buchner, E. (1996). Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J. Neurosci. 16, 3154-3165.
23. Kurylas, A. E., Rohlfing, T., Krofczik, S., Jenett, A., and Homberg, U. (2008). Standardized atlas of the brain of the desert locust, Schistocerca gregaria. Cell Tissue Res. 333, 125-145.
24. Kuß, A., Hege, H. C., Krofczik, S., and Borner, J. (2007). Pipeline for the creation of surface-based averaged brain atlases. In Proceedings of Winter School of Computer Graphics 2007, 1, 17-24.
25. Kvello, P., Løfaldli, B. B., Rybak, J., Menzel, R., and Mustaparta, H. (2009). Digital, three-dimensional average shaped atlas of the Heliothis virescens brain with integrated gustatory and olfactory neurons. Front. Syst. Neurosci. 3:14. doi: 10.3389/neuro.06.014.2009.
26. Labhart, T. (1988). Polarization-opponent interneurons in the insect visual system. Nature 331, 435-437.
27. Labhart, T., and Meyer, E. P. (1999). Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc. Res. Tech. 47, 368-379.
28. Labhart, T., Petzold, J., and Helbling, H. (2001). Spatial integration in polarization- sensitive interneurones of crickets: a survey of evidence, mechanisms and benefits. J. Exp. Biol. 204, 2423-2430.
29. Liu, G., Seiler, H., Wen, A., Zars, T., Ito, K., Wolf, R., Heisenberg, M., and Liu, L. (2006). Distinct memory traces for two visual features in the Drosophila brain. Nature 439, 551-556.
30. Mappes, M., and Homberg, U. (2004). Behavioral analysis of polarization vision in tethered flying locusts. J. Comp. Physiol. A 190, 61-68.
31. Müller, M. (1997). Anatomische und funktionelle Charakterisierung der unteren Einheit des Zentralkörpers im Gehirn der Heuschrecke Schistocerca gregaria. Doctoral Thesis, Universität Regensburg, Germany.
32. Müller, M., Homberg, U., and 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.
33. Neuser, K., Triphan, T., Mronz, M., Poeck, B., and Strauss, R. (2008). Analysis of a spatial orientation memory in Drosophila. Nature 453, 1244-1247.
34. Ott, S. R. (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.
35. Pfeiffer, K., and Homberg, U. (2007). Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr. Biol. 17, 960-965.
36. Pfeiffer, K., Kinoshita, M., and 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.
37. Poeck, B., Triphan, T., Neuser, K., and Strauss, R. (2008). Locomotor control by the central complex in Drosophila - An analysis of the tay bridge mutant. Dev. Neurobiol. 68, 1046-1058.
38. Rein, K., Zöckler, M., Mader, M. T., Grübel, C., and Heisenberg, M. (2002). The Drosophila standard brain. Curr. Biol. 12, 227-231.
39. Rohlfing, T., Brandt, R., Maurer, C. R. Jr, and 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. 187-194.
40. Rohlfing, T., Brandt, R., Menzel, R., and Maurer, C. R. (2004). Evaluation of atlas selection strategies for atlasbased image segmentation with application to confocal microscopy images of bee brains. Neuroimage 21, 1428-1442.
41. Sakura, M., Lambrinos, D., and Labhart, T. (2008). Polarized skylight navigation in insects: model and electrophysiology of e-vector coding by neurons in the central complex. J. Neurophysiol. 99, 667-682.
42. Schmitt, S., Evers, J. F., Duch, C., Scholz, M., and Obermayer, K. (2004). New methods for the computer-assisted 3-D reconstruction of neurons from confocal image stacks. Neuroimage 23, 1283-1298.
43. Siegl, T., Schachtner, J., Holstein, G. R., and Homberg, U. (2009). NO/ cGMP signalling: L-citrulline and cGMP immunostaining in the central complex of the desert locust Schistocerca gregaria. Cell Tissue Res. 337, 327-340.
44. Strausfeld, N. J. (1976). Atlas of an Insect Brain. Heidelberg, Springer.
45. Strauss, R. (2002). The central complex and the genetic dissection of locomotor behaviour. Curr. Opin. Neurobiol. 12, 633-638.
46. Strauss, R., and Heisenberg, M. (1993). A higher control center of locomotor behavior in the Drosophila brain. J. Neurosci. 13, 1852-1861.
47. Vitzthum, H., Müller, M., and Homberg, U. (2002). Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J. Neurosci. 22, 1114-1125.
48. Wang, Z., Pan, Y., Li, W., Jiang, H., Chatzimanolis, L., Chang, J., Gong, Z., and Liu, L. (2008). Visual pattern memory requires foraging function in the central complex of Drosophila. Learn. Mem. 15, 133-142.
49. Wehner, R. (1992). Arthropods. In Animal Homing, F. Papi, ed. (London, Chapman and Hall), pp. 45-144.
50. Williams, J. L. D. (1972). Some Observations on the Neuronal Organisation of the Supra-Oesophageal Ganglion in Schistocerca gregaria Forskål with Particular Reference to the Central Complex. PhD Thesis, University of Wales, Cardiff
51. Williams, J. L. D. (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. 176, 67-86.