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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Bausenwein B (1988) Neuronale Aktivitätsmarkierung während visueller Flugsteuerung von Drosophila melanogaster. Dissertation, Universität Würzburg
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 3:87–109
Buchner E (1976) Elementary movement detectors in an insect visual system. Biol Cybern 24:85–101
Buchner E, Buchner S, Bülthoff I (1984) Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. J Comp Physiol 155: 471–483
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 13:1–168
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 31–36
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 52:195–209
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 11:351–358
Fischbach K-F (1979) Simultaneous and successive colour contrast expressed in “slow” phototactic behaviour of walking Drosophila melanogaster. J Comp Physiol 130:161–171
Fischbach K-F (1983) Neurogenetik am Beispiel des visuellen Systems von Drosophila melanogaster. Habilitation Thesis, Universität Würzburg
Fischbach K-F, Dittrich APM (1989) The optic lobe of Drosophila melanogaster. Part I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441–475
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 4:444–463
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 18:343–357
Fukushi T, (1989) Learning and discrimination of coloured papers in the walking blowfly, Lucilia cuprina. J Comp Physiol A 166:57–64
Fukushi T (1990) Colour discrimination from various shades of grey in the trained blowfly, Lucilia cuprina. J Insect Physiol 36:69–75
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: 141–149
Hardie RC (1986) The photoreceptor array of the dipteran retina. Trends Neurosci 9:419–423
Harris WS, Stark WS, Walker JA (1976) Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster. J Physiol (Lond) 256:415–439
Hausen K, (1981) Monocular and binocular computation of motion in the lobula plate of the fly. Verh Dtsch Zool Ges 1981:49–70
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 391–424
Hausen K, Wehrhahn C (1983) Microsurgical lesion of horizontal cells changes optomotor yaw responses in the blowfly, Proc R Soc Lond (Biol) 219:211–216
Heisenberg M, Buchner E (1977) The role of retinula cell types in visual behavior of Drosophila melanogaster. J Comp Physiol 117:127–162
Hertel H (1980) Chromatic properties of identified interneurons in the optic lobes of the bee. J Comp Physiol 137:215–231
Hu KG, Stark WS (1977) Specific receptor input into spectral preference in Drosophila. J Comp Physiol 121:241–252
Ilse D (1949) Colour discrimination in the dronefly, Eristalis tenax. Nature 163:255–256
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 359–377
Kien J, Menzel R (1977a) Chromatic properties in the optic lobes of the bee. I. Broad band neurons. J Comp Physiol 113:17–34
Kien J, Menzel R (1977b) Chromatic properties in the optic lobes of the bee. II. Narrow band and colour opponent neurons. J Comp Physiol 113:35–53
Kirschfeld K, Feiler R, Franceschini N (1978) A photostable pigment within the rhabdomere of fly photoreceptors no. 7. J Comp Physiol 125:275–284
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 457–481
Livingston M, Hubel D (1988) Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240:740–749
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 305:232–263
Menne D, Spatz H-C (1977) Color vision in Drosophila melanogaster. J Comp Physiol 114:301–312
Miller JP, Jacobs GA (1984) Relationships between neuronal structure and function. J Exp Biol 112:129–145
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)
Reichardt W, Poggio T (1976) Visual control of orientation behaviour in the fly. I. A quantitative analysis of neural interactions. Q Rev Biophys 9:311–375
Schürmann FW (1974) Bemerkungen zur Funktion der Corpora pedunculata im Gehirn der Insekten aus morphologischer Sicht. Exp Brain Res 19:406–432
Shaw SR (1984) Early visual processing in insects. J Exp Biol 112:225–251
Srinivasan MV, Guy RG (1990) Spectral properties of movement perception in the dronefly Eristalis. J Comp Physiol A 166:287–295
Strausfeld NJ (1970) Golgi studies on insects. II. The optic lobes of Diptera. Philos Trans R Soc Lond 258:135–223
Strausfeld NJ (1971) The organization of the insect visual system (light microscopy). II. The projection of fibres across the first optic chiasm. Z Zellforsch 121:442–454
Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York
Strausfeld NJ (1984) Functional neuroanatomy of the blowfly's visual system. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 483–522
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 319–353
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 317–359
Strausfeld NJ, Lee J-K (1991) Neuronal basis for parallel visual processing in the fly. Visual Neuroscience 7:13–33
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 141–176
Tinbergen J, Abeln RG (1983) Spectral sensitivity of the landing blowfly. J Comp Physiol 150:319–328
Author information
Authors and Affiliations
Additional information
During the final editing of this work our friend A.P.M. Dittrich was tragically killed in an accident. Without him this and the previous work would never have been completed
Rights and permissions
About this article
Cite this article
Bausenwein, B., Dittrich, A.P.M. & Fischbach, K.F. The optic lobe of Drosophila melanogaster . Cell Tissue Res 267, 17–28 (1992). https://doi.org/10.1007/BF00318687
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00318687