Cell and Tissue Research

, Volume 267, Issue 1, pp 17–28 | Cite as

The optic lobe of Drosophila melanogaster

II. Sorting of retinotopic pathways in the medulla
  • B. Bausenwein
  • A. P. M. Dittrich
  • K. -F. Fischbach
Article

Summary

We present a quantitative evaluation of Golgiimpregnated columnar neurons in the optic lobe of wildtype Drosophila melanogaster. This analysis reveals the overall connectivity pattern between the 10 neuropil layers of the medulla and demonstrates the existence of at least three major visual pathways. Pathway 1 connects medulla layer M10 to the lobula plate. Input layers of this pathway are M1 and M5. Pathway 2 connects M9 to shallow layers of the lobula, which in turn are tightly linked to the lobula plate. This pathway gets major input via M2. Pathways 1 and 2 receive input from retinula cells R1-6, either via the lamina monopolar cell L1 (terminating in M1 and M5) or via L2 and T1 (terminating in M2). Neurons of these pathways typically have small dendritic fields. We discuss evidence that pathways 1 and 2 may play a major role in motion detection. Pathway 3 connects M8 to deep layers of the lobula. In M8 information converges that is derived either from M3 (pathway 3a) or from M4 and M6 (pathway 3b), layers that get their major input from L3 and R8 or L4 and R7, respectively. Some neurons of pathway 3 have large dendritic fields. We suggest that they may be involved in the computation of form and colour. Possible analogies to the organization of pathways in the visual system of vertebrates are discussed.

Key words

Visual system Optic lobe Medulla Retinotopic pathways Motion detection Colour vision Drosophila melanogaster (Insecta) 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bausenwein B (1988) Neuronale Aktivitätsmarkierung während visueller Flugsteuerung von Drosophila melanogaster. Dissertation, Universität WürzburgGoogle Scholar
  2. Bausenwein B, Wolf R, Heisenberg M (1986) Genetic dissection of optomotor behavior in Drosophila melanogaster: studies on wild type and the mutant optomotor-blindH31. J Neurogenet 3:87–109Google Scholar
  3. Buchner E (1976) Elementary movement detectors in an insect visual system. Biol Cybern 24:85–101Google Scholar
  4. Buchner E, Buchner S, Bülthoff I (1984) Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. J Comp Physiol 155: 471–483Google Scholar
  5. Cajal SR, Sánchez D (1915) Contribucion al conocimiento de los centros nerviosos de los insectos. Parte I, retina y centros opticos. Trab Lab Invest Bil Univ Madr 13:1–168Google Scholar
  6. Campos-Ortega JA, Strausfeld N (1972) Columns and layers in the second synaptic region of the fly's visual system: the case for two superimposed neuronal architectures. In: Wehner R (ed) Information processing in the visual system of arthropods. Springer, Berlin Heidelberg New York, pp 31–36Google Scholar
  7. Egelhaaf M (1985) On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. II. Figure detection cells, a new class of visual interneurons. Biol Cyberr 52:195–209Google Scholar
  8. Egelhaaf M, Hausen K, Reichardt W, Wehrhahn C (1988) Visual course control in flies relies on neuronal computation of object and background motion. Trends Neurosci 11:351–358Google Scholar
  9. Fischbach K-F (1979) Simultaneous and successive colour contrast expressed in “slow” phototactic behaviour of walking Drosophila melanogaster. J Comp Physiol 130:161–171Google Scholar
  10. Fischbach K-F (1983) Neurogenetik am Beispiel des visuellen Systems von Drosophila melanogaster. Habilitation Thesis, Universität WürzburgGoogle Scholar
  11. Fischbach K-F, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. Part I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441–475Google Scholar
  12. Fortini ME, Rubin GM (1990) Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. Genes Dev 4:444–463Google Scholar
  13. Fröhlich A, Meinertzhagen IA (1987) Regulation of synaptic frequency: comparison of the effects of hypoinnervation with those of hyperinnervation in the fly's compound eye. J Neurobiol 18:343–357Google Scholar
  14. Fukushi T, (1989) Learning and discrimination of coloured papers in the walking blowfly, Lucilia cuprina. J Comp Physiol A 166:57–64Google Scholar
  15. Fukushi T (1990) Colour discrimination from various shades of grey in the trained blowfly, Lucilia cuprina. J Insect Physiol 36:69–75Google Scholar
  16. Geiger G, Nässel DR (1982) Visual processing of single objects and wide-field patterns in flies: behavioural analysis after laser-surgical removal of interneurons. Biol Cybern 44: 141–149Google Scholar
  17. Hardie RC (1986) The photoreceptor array of the dipteran retina. Trends Neurosci 9:419–423Google Scholar
  18. Harris WS, Stark WS, Walker JA (1976) Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster. J Physiol (Lond) 256:415–439Google Scholar
  19. Hausen K, (1981) Monocular and binocular computation of motion in the lobula plate of the fly. Verh Dtsch Zool Ges 1981:49–70Google Scholar
  20. Hausen K, Egelhaaf M (1989) Neural mechanisms of visual course control in insects. In: Stavenga DG, Hardie R (eds) Facets of vision. Springer, Berlin Heidelberg New York pp 391–424Google Scholar
  21. Hausen K, Wehrhahn C (1983) Microsurgical lesion of horizontal cells changes optomotor yaw responses in the blowfly, Proc R Soc Lond (Biol) 219:211–216Google Scholar
  22. Heisenberg M, Buchner E (1977) The role of retinula cell types in visual behavior of Drosophila melanogaster. J Comp Physiol 117:127–162Google Scholar
  23. Hertel H (1980) Chromatic properties of identified interneurons in the optic lobes of the bee. J Comp Physiol 137:215–231Google Scholar
  24. Hu KG, Stark WS (1977) Specific receptor input into spectral preference in Drosophila. J Comp Physiol 121:241–252Google Scholar
  25. Ilse D (1949) Colour discrimination in the dronefly, Eristalis tenax. Nature 163:255–256Google Scholar
  26. Kaiser W (1975) The relationship between visual movement detection and colour vision in insects. In: Horridge GA (ed) The compound eye and vision of insects. Clarendon, Oxford, pp 359–377Google Scholar
  27. Kien J, Menzel R (1977a) Chromatic properties in the optic lobes of the bee. I. Broad band neurons. J Comp Physiol 113:17–34Google Scholar
  28. Kien J, Menzel R (1977b) Chromatic properties in the optic lobes of the bee. II. Narrow band and colour opponent neurons. J Comp Physiol 113:35–53Google Scholar
  29. Kirschfeld K, Feiler R, Franceschini N (1978) A photostable pigment within the rhabdomere of fly photoreceptors no. 7. J Comp Physiol 125:275–284Google Scholar
  30. Laughlin S (1984) The roles of parallel channels in early visual processing by the arthropod eye. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, pp 457–481Google Scholar
  31. Livingston M, Hubel D (1988) Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240:740–749Google Scholar
  32. Meinertzhagen IA, O'Neil SD (1991) The synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster J Comp Neurol 305:232–263Google Scholar
  33. Menne D, Spatz H-C (1977) Color vision in Drosophila melanogaster. J Comp Physiol 114:301–312Google Scholar
  34. Miller JP, Jacobs GA (1984) Relationships between neuronal structure and function. J Exp Biol 112:129–145Google Scholar
  35. Osorio D (1991) Patterns of function and evolution in the arthropod optic lobe. In: Cronly-Dillon JR, Gregory RL (eds) Vision and visual dysfunction. II. Evolution of the eye and visual system. Macmillan, London (In press)Google Scholar
  36. Reichardt W, Poggio T (1976) Visual control of orientation behaviour in the fly. I. A quantitative analysis of neural interactions. Q Rev Biophys 9:311–375Google Scholar
  37. Schürmann FW (1974) Bemerkungen zur Funktion der Corpora pedunculata im Gehirn der Insekten aus morphologischer Sicht. Exp Brain Res 19:406–432Google Scholar
  38. Shaw SR (1984) Early visual processing in insects. J Exp Biol 112:225–251Google Scholar
  39. Srinivasan MV, Guy RG (1990) Spectral properties of movement perception in the dronefly Eristalis. J Comp Physiol A 166:287–295Google Scholar
  40. Strausfeld NJ (1970) Golgi studies on insects. II. The optic lobes of Diptera. Philos Trans R Soc Lond 258:135–223Google Scholar
  41. Strausfeld NJ (1971) The organization of the insect visual system (light microscopy). II. The projection of fibres across the first optic chiasm. Z Zellforsch 121:442–454Google Scholar
  42. Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New YorkGoogle Scholar
  43. Strausfeld NJ (1984) Functional neuroanatomy of the blowfly's visual system. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 483–522Google Scholar
  44. Strausfeld NJ (1989a) Insect vision and olfaction: common design principles of neuronal organization. In: Singh RN, Strausfeld NJ (eds) Neurobiology of sensory systems. Plenum, New York, pp 319–353Google Scholar
  45. Strausfeld NJ (1989b) Beneath the compound eye: neuroanatomical analysis and physiological correlates in the study of insect vision. In: Stavenga DG, Hardie r (eds) Facets of vision. Springer, Berlin Heidelberg New York, pp 317–359Google Scholar
  46. Strausfeld NJ, Lee J-K (1991) Neuronal basis for parallel visual processing in the fly. Visual Neuroscience 7:13–33Google Scholar
  47. Szentágothai J (1973) Neuronal and synaptic architecture of the lateral geniculate nucleus. In: Jung R (ed) Handbook of sensory physiology, vol VI B. Central visual information. Springer, Berlin Heidelberg New York, pp 141–176Google Scholar
  48. Tinbergen J, Abeln RG (1983) Spectral sensitivity of the landing blowfly. J Comp Physiol 150:319–328Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • B. Bausenwein
    • 1
  • A. P. M. Dittrich
    • 1
  • K. -F. Fischbach
    • 1
  1. 1.Institut für Biologie IIIFreiburg i. Br.Federal Republic of Germany

Personalised recommendations