Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T08:26:18.843Z Has data issue: false hasContentIssue false
  • English
  • Français

Sign-conserving amacrine neurons in the fly's external plexiform layer

Published online by Cambridge University Press:  02 August 2005

JOHN K. DOUGLASS  and
NICHOLAS J. STRAUSFELD
JOHN K. DOUGLASS
Affiliation:
Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson
NICHOLAS J. STRAUSFELD
Affiliation:
Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson
Get access Rights & Permissions [Opens in a new window]

Abstract

Amacrine cells in the external plexiform layer of the fly's lamina have been intracellulary recorded and dye-filled for the first time. The recordings demonstrate that like the lamina's short photoreceptors R1–R6, type 1 lamina amacrine neurons exhibit nonspiking, “sign-conserving” sustained depolarizations in response to illumination. This contrasts with the sign-inverting responses that typify first-order retinotopic relay neurons: monopolar cells L1–L5 and the T1 efferent neuron. The contrast frequency tuning of amacrine neurons is similar to that of photoreceptors and large lamina monopolar cells. Initial observations indicate that lamina amacrine receptive fields are also photoreceptor-like, suggesting either that their inputs originate from a small number of neighboring visual sampling units (VSUs), or that locally generated potentials decay rapidly with displacement. Lamina amacrines also respond to motion, and in one recording these responses were selective for the orientation of moving edges. This functional organization corresponds to the anatomy of amacrine cells, in which postsynaptic inputs from several neighboring photoreceptor endings are linked by a network of very thin distal processes. In this way, each VSU can receive convergent inputs from a surround of amacrine processes. This arrangement is well suited for relaying responses to local intensity fluctuations from neighboring VSUs to a central VSU where amacrines are known to be presynaptic to the dendrites of the T1 efferent. The T1 terminal converges at a deeper level with that of the L2 monopolar cell relaying from the same optic cartridge. Thus, the localized spatial responses and receptor-like temporal response properties of amacrines are consistent with possible roles in lateral inhibition, motion processing, or orientation processing.

Keywords

Early visual processingElementary motion detectionReceptive fieldsPhotoreceptorsDiptera
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 3 , May 2005 , pp. 345 - 358
Copyright
2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, J.C. & Laughlin, S.B. (2000). Photoreceptor performance and the co-ordination of achromatic and chromatic inputs to the fly visual system. Vision Research 40, 13–31.Google Scholar
Bloomfield, S.A. & Dacheux, R.F. (2001). Rod vision: Pathways and processing in the mammalian retina. Progress in Retinal and Eye Research 20, 351–384.Google Scholar
Boschek, C.B. (1971). On the fine structure of the peripheral retina and the lamina of the fly, Musca domestica. Zeitschrift für Zellforschung und Mikroskopische Anatomie 110, 369–409.Google Scholar
Braitenberg, V. (1967). Patterns of projection in the visual system of the fly. I. Retina-lamina projections. Experimental Brain Research 3, 271–298.Google Scholar
Burkhardt, D. & Autrum, H. (1960). Die Belichtungspotentiale einzelner Sehzellen von Calliphora erythrocephala Meig. Zeitschrift für Naturforschung 15b, 612–616.Google Scholar
Burton, B.G., Tatler, B.W., & Laughlin, S.B. (2001). Variations in photoreceptor response dynamics across the fly retina. Journal of Neurophysiology 86, 950–960.Google Scholar
Buschbeck, E.K. & Strausfeld, N.J. (1996). Visual motion-detection circuits in flies: Small-field retinotopic elements responding to motion are evolutionarily conserved across taxa. Journal of Neuroscience 16, 4563–4578.Google Scholar
Campos-Ortega, J.A. & Strausfeld, N.J. (1973). Synaptic connections of intrinsic cells and basket arborizations in the external plexiform layer of the fly's eye. Brain Research 59, 119–136.Google Scholar
Coombe, P., Srinivasan, M.V., & Guy, R.G. (1989). Are the large monopolar cells of the insect lamina on the optomotor pathway? Journal of Comparative Physiology A 166, 23–35.Google Scholar
Douglass, J.K. & Strausfeld, N.J. (1995). Visual motion detection circuits in flies: Peripheral motion computation by identified small-field retinotopic neurons. Journal of Neuroscience 15, 5596–5611.Google Scholar
Douglass, J.K. & Strausfeld, N.J. (1996). Visual motion-detection circuits in flies: Parallel direction- and non-direction-sensitive pathways between the medulla and lobula plate. Journal of Neuroscience 16, 4551–4562.Google Scholar
Douglass, J.K. & Strausfeld, N.J. (1998). Functionally and anatomically segregated visual pathways in the lobula complex of a calliphorid fly. Journal of Comparative Neurology 396, 84–104.Google Scholar
Douglass, J.K. & Strausfeld, N.J. (2003a). Anatomical organization of retinotopic motion-sensitive pathways in the optic lobes of flies. Microscopy Research and Technique 62, 132–150.Google Scholar
Douglass, J.K. & Strausfeld, N.J. (2003b). Retinotopic pathways providing motion-selective information to the lobula from peripheral elementary motion detecting circuits. Journal of Comparative Neurology 456, 326–344.Google Scholar
Franceschini, N. (1975). Sampling of the visual environment by the compound eye of the fly: Fundamentals and applications. In Photoreceptor Optics, ed. Snyder, A.W. & Menzel, R., pp. 8–125. Berlin, Heidelberg, New York: Springer.
Geng, C., Leung, H.-T,, Skingsley, D.R., Iovchev, M.I., Yin, Z., Semenov, E.P,, Burg, M.G., Hardie, R.C., & Pak, W.L. (2002). The target of Drosophila photoreceptor synaptic transmission is a histamine-gated chloride channel encoded by ort (hclA). Journal of Biological Chemistry 277, 42113–42120.Google Scholar
Gilbert, C., Penisten, D.K., & DeVoe, R.D. (1991). Discrimination of visual motion from flicker by identified neurons in the medulla of the fleshfly Sarcophaga bullata. Journal of Comparative Physiology A 168, 653–673.Google Scholar
Hardie, R.C. (1979). Electrophysiological analysis of fly retina. I. Comparative properties of R1-R6 and R7 and 8. Journal of Comparative Physiology A 129, 19–33.Google Scholar
Hardie, R.C. (1986). The photoreceptor array of the dipteran retina. Trends in Neuroscience 9, 419–423.Google Scholar
Hardie, R.C. (1989). A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature (London) 339, 704–706.Google Scholar
Hengstenberg, R. (1982). Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. Journal of Comparative Physiology 149, 179–193.Google Scholar
Higgins, C.M., Douglass, J.K., & Strausfeld, N.J. (2004). The computational basis of an identified neuronal circuit for elementary motion detection in dipterous insects. Visual Neuroscience 21, 567–586.Google Scholar
Ioannides, A.C. (1972) Light adaptation and signal transmission in the compound eye of the giant water bug Lethocerus (Belastomatidae: Hemiptera). Ph.D. Thesis, Canberra National University, Australia.
Järvilehto, M. & Zettler, F. (1973). Electrophysiological-histological studies on some functional properties of visual cells and second-order neurons of an insect retina. Zeitschrift für Zellforschung und Mikroskopische Anatomie 136, 291–306.Google Scholar
Juusola, M., Kouvalainen, E., Järvilehto, M., & Weckström, M. (1994). Contrast gain, signal-to-noise ratio, and linearity in light-adapted blowfly photoreceptors. Journal of General Physiology 104, 593–621.Google Scholar
Kral, K. & Schneider, L. (1981). Fine structural localisation of acetylcholinesterase activity in the compound eye of the honeybee (Apis mellifica L.). Cell and Tissue Research 221, 351–359.Google Scholar
Lamb, T.D. (1976). Spatial properties of horizontal cell responses in the turtle retina. Journal of Physiology 263, 239–255.Google Scholar
Laughlin, S.B. (1981). Neural principles in the peripheral visual systems of invertebrates. In Handbook of Sensory Physiology, VII/6B, ed. Autrum, H., pp. 133–280. Berlin: Springer.
Laughlin, S.B. & Hardie, R.C. (1978). Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. Journal of Comparative Physiology 128, 319–340.Google Scholar
Meinertzhagen, I.A. & O'Neil, S.D. (1991). Synaptic organization of columnar elements in the lamina of the wild-type in Drosophila melanogaster. Journal of Comparative Neurology 305(2), 232–263.Google Scholar
Naka, K.I. & Rushton, W.A.H. (1967). The generation and spread of s-potentials in fish (cyprinidae). Journal of Physiology 192, 437–461.Google Scholar
Nässel, D.R. (1999). Histamine in the brain of insects: A review. Microscopy Research and Technique 44, 121–136.Google Scholar
Nässel, D.R., Holmqvist, M.H., Hardie, R.C., Hakanson, R., & Sundler, F. (1988). Histamine-like immunoreactivity in photoreceptors of the compound eyes and ocelli of the flies Calliphora erythrocephala and Musca domestica. Cell and Tissue Research 253, 639–646.Google Scholar
O'Shea, M. & Adams, M.E. (1981). Pentapeptide (proctolin) associated with an identified neuron. Science 21, 567–569.Google Scholar
Quian, H. & Ripps, H. (1992). Receptive-field properties of rod-driven horizontal cells in the skate retina. Journal of General Physiology 100, 457–478.Google Scholar
Roeder, T. (2003). Metabotropic histamine receptors—nothing for invertebrates? European Journal of Pharmacology 466, 85–90.Google Scholar
Scholes, J. (1969). The electrical responses of the retinal receptors and the lamina in the visual system of the fly Musca. Kybernetik 6, 149–162.Google Scholar
Scholes, J. & Reichardt, W. (1969). The quantal content of optomotor stimuli and the electrical responses of receptors in the compound eye of the fly Musca. Kybernetik 6, 74–79.Google Scholar
Shaw, S.R. (1981). Anatomy and physiology of identified non-spiking cells in the photoreceptor-lamina complex of the compound eye of insects, especially Diptera. In Neurones Without Impulses: Their Significance for Vertebrate and Invertebrate Nervous Systems, eds. Roberts, A. & Bush, B.M.H., pp. 61–116. Cambridge: Cambridge University Press.
Shaw, S.R. (1984). Early visual processing in insects. Journal of Experimental Biology 112, 225–251.Google Scholar
Sinakevitch, I. & Strausfeld, N.J. (2004). Chemical neuroanatomy of the fly's movement detection pathway. Journal of Comparative Neurology 468, 6–23.Google Scholar
Smakman, J.G.J., van Hateren, J.H., & Stavenga, D.G. (1984). Angular sensitivity of blowfly photoreceptors: Intracellular measurements and wave-optical predictions. Journal of Comparative Physiology A 155, 239–247.Google Scholar
Strausfeld, N.J. (1970). Golgi studies on insects. Part II. The optic lobes of Diptera. Philosophical Transactions of the Royal Society B (London) 258, 135–223.Google Scholar
Strausfeld, N.J. (1976). Mosaic organizations, layers, and visual pathways in the insect brain. In Neural Principles in Vision, ed. Zettler, F. & Weiler, R., pp. 245–279. Berlin, Heidelberg, New York: Springer.
Strausfeld, N.J. (1989). Beneath the compound eye: Neuroanatomical analysis and physiological correlates in the study of insect vision. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 317–359. Heidelberg: Springer.
Strausfeld, N.J. & Campos-Ortega, J.A. (1977). Vision in insects: Pathways possibly underlying neural adaptation and lateral inhibition. Science 195, 894–897.Google Scholar
Strausfeld, N.J. & Li, Y. (1999). Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies. Journal of Comparative Neurology 409, 603–625.Google Scholar
Strausfeld, N.J. & Nässel, D.R. (1980). Neuroarchitecture of brain regions that subserve the compound eyes of Crustacea and Insects. In Handbook of sensory physiology, VII/6B, ed. Autrum, H., pp. 1–133. Heidelberg: Springer.
Stuart, A.E. (1999). From fruit flies to barnacles, histamine is the neurotransmitter of arthropod photoreceptors. Neuron 22, 431–433.Google Scholar
Tomita, T. (1965). Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harbor Symposia on Quantitative Biology 30, 559–566.Google Scholar
Washizu, Y., Burkhardt, D., & Streck, P. (1964). Visual field of single retinula cells and interommatidial inclination in the compound eye of the blowfly Calliphora erythrocephala. Zeitschrift für Vergleichende Physiologie 48, 413–428.Google Scholar
Wolfgang, W.J. & Forte, M.A. (1989). Expression of acetylcholinesterase during visual system development in Drosophila. Developmental Biology 131, 321–330.Google Scholar
Yasuyama, K. & Meinertzhagen, I.A. (1999). Extraretinal photoreceptors at the compound eye's posterior margin in Drosophila melanogaster. Journal of Comparative Neurology 412, 193–202.Google Scholar
Zettler, F. & Weiler, R. (1976). Neuronal processing in the first optic neuropile of the compound eye of the fly. In Neural Principles in Vision, ed. Zettler, F. & Weiler, R., pp. 227–237. New York: Springer.