Advertisement

Journal of comparative physiology

, Volume 143, Issue 4, pp 511–526 | Cite as

The horizontal cells in the lobula plate of the blowfly,Phaenicia sericata

  • Hendrik Eckert
Article

Summary

Summary

Combining intracellular recording and dye injection techniques, the horizontal cells of the blowfly,Phaenicia (= Lucilia) sericata, were studied.

Anatomy

In each lobula plate, one finds a set of three cells, termed NH-, EH- and SH-cell. EH occurs in two distinct anatomical forms, EH1 and EH2, differing in their respective branching patterns of the axon at the frontal surface of the lobula plate. Each cell's dendrite covers approximately a third of the surface of the lobula plate corresponding to a third of the visual field of the ipsilateral eye. These dendrites possess postsynaptic spines. The axons of all three cells pass along the frontal surface of the lobula plate within the inner chiasma; they cross the optic peduncle and enter the central protocerebrum where they form a second arborization, the axonal arborization consisting of dorsally extending collaterals. The axons terminate in the posterior slope of the ventrolateral protocerebrum. The axonal arborization as well as the axonal terminals possess telodendritic knobs. Ultrastructural investigations show that the lobula plate-dendrite possesses exclusively postsynaptic chemical synapses, and that the axonal arborisation and the axonal terminals possess pre- as well as postsynaptic chemical synapses. The very endings of the axons are exclusively presynaptic.

Physiology

The horizontal cells respond to stimulation within the ipsi- and/or contralateral receptive field. Regressive motion within the contralateral receptive field induces EPSPs and action potentials of small amplitude (10–35 mV); progressive motion is ineffective. Within the ipsilateral receptive field, regressive motion hyperpolarizes the cell membrane whereas progressive motion induces a strong depolarizing membrane potential-shift with superimposed fast potential changes of ‘noisy’ appearance. Thus, the horizontal cells respond to rotational movement of the surround around the high axis of the animal: clockwise rotation excites the horizontal cells of the right lobula plate and counterclockwise motion those of the left lobula plate, respectively. However, this compound potential behaviour can only be recorded in the lobula plate-axon and main dendrites, whereas the horizontal cells respond tocontralateral regressive motion with action potentialsonly in their axonal terminals in the posterior slope; no graded potentials can be recorded in this cell region if stimulation occurs within theipsilateral receptive field. It is discussed that the previously described graded potentials for the axonal terminals (Hausen 1976b) can only be measured if the cells are already damaged. The probable cause of this change in response behaviour from action potentials to a compound potential behaviour (consisting of graded potentials and action potentials though of small amplitude) is discussed.

Keywords

Receptive Field Frontal Surface Axonal Terminal Horizontal Cell Progressive Motion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bacon J, Altman J (1977) A silver intensification method for cobaltfilled neurones in wholemount preparations. Brain Res 138:359–363Google Scholar
  2. Beersma DGM, Stavenga DG, Kuiper JW (1975) Organization of visual axes in the compound eye of the flyMusca domestica L. and behavioural consequences. J Comp Physiol 102:305–320Google Scholar
  3. Bishop LG, Keehn DG (1966) Two types of motion sensitive neurons in the fly optic lobe. Nature 212:1374–1376Google Scholar
  4. Braitenberg V (1970) Ordnung und Orientierung der Elemente im Sehsystem der Fliege. Kybernetik 7:235–242Google Scholar
  5. Campos-Ortega J, Strausfeld NJ (1972) The columnar organization of the second synaptic region of the visual system ofMusca domestica L. I. Receptor terminals in the medulla. Z Zellforsch 124:561–585Google Scholar
  6. Cole KS, Curtis HJ (1939) Electric impedance of squid giant axon during activity. J Gen Physiol 22:649–670Google Scholar
  7. Collett TS, Land MF (1975) Visual control of flight behaviour in the hoverfly,Syritta pipiens L. J Comp Physiol 99:1–66Google Scholar
  8. Dvorak DR, Bishop LG, Eckert HE (1975) On the identification of movement detectors in the fly optic lobe. J Comp Physiol 100:5–23Google Scholar
  9. Ebbesson SOE (1970) In: Nauta WJH, Ebbesson SOE (eds) Contemporary research methods in neuroanatomy. Springer, Berlin Heidelberg New York, p 157Google Scholar
  10. Eckert H, (1973) Optomotorische Untersuchungen am visuellen System der StubenfliegeMusca domestica L. Kybernetik 14:1–23Google Scholar
  11. Eckert H (1976) Identifizierte, bewegungssensitive Interneurone als neurophysiologische Korrelate für das Bewegungssehen der Insekten. Verh Dtsch Zool Ges 1976:253Google Scholar
  12. Eckert H (1977) Identification of horizontal and vertical movement detection systems in insects. Abstract, Soc Neurosci Ann Meeting, Los AngelesGoogle Scholar
  13. Eckert H (1978) Response properties of dipteran giant visual interneurones involved in control of optomotor behaviour. Nature 271:358–360Google Scholar
  14. Eckert H (1979) Anatomie, Elektrophysiologie und funktionelle Bedeutung bewegungssensitiver Neurone in der Sehbahn von Insekten (Phaenicia). Habilitationsschrift, Universität BochumGoogle Scholar
  15. Eckert H (1980a) Response properties of the H1-neurone in the third optic ganglion of the blowfly,Phaenicia. J Comp Physiol 135:29–39Google Scholar
  16. Eckert H (1980b) Orientation sensitivity of the visual movement detection system activating the landing response of the blowfliesCalliphora andPhaenicia: a behavioural investigation. Biol Cybern 37:235–247Google Scholar
  17. Eckert H, Bishop LG (1976) Response properties of identified visual interneurones in the third optic ganglion of dipterans (Phaenicia sericata) in the context of behavioural responses. Abstract, Soc Neurosci Ann Meeting, TorontoGoogle Scholar
  18. Eckert H, Bishop LG (1978) Anatomical and physiological properties of the ‘vertical cells’ in the third optic ganglion of the blowfly,Phaenicia sericata (Calliphoridae, Diptera). J Comp Physiol 126:57–86Google Scholar
  19. Eckert H, Boschek CB (1980) In: Strausfeld NJ, Miller TW (eds) Experimental entomology, vol I, Neuroanatomical techniques. Springer, Berlin Heidelberg New York, pp 325–339Google Scholar
  20. Eckert H, Hamdorf K (1981) Action potentials in non-spiking neurones. Z Naturforsch 36c:470–474Google Scholar
  21. Eckert H, Meller K (1981) Synaptic structures of identified motion-sensitive neurones in the brain of the fly,Phaenicia. Verh Dtsch Zool Ges 1981 (in press)Google Scholar
  22. Götz KG (1964) Optomotorische Untersuchungen des visuellen Systems einiger Augenmutanten der FruchtfliegeDrosophila. Kybernetik 2:215–221Google Scholar
  23. Hausen K (1976a) Funktion, Struktur und Konnektivität bewegungsempfindlicher Interneurone in der Lobula Platte von Dipteren. Verh Dtsch Zool Ges 1976:65Google Scholar
  24. Hausen K (1976b) Functional characterization and anatomical identification of motion sensitive neurones in the lobula plate of the blowflyCalliphora erythrocephala. Z Naturforsch 31c:629–633Google Scholar
  25. Hausen K (1976c) Struktur, Funktion und Konnektivität bewegungsempfindlicher Interneurone im dritten optischen Neuropil der SchmeißfliegeCalliphora erythrocephala. Dissertation, Universität TübingenGoogle Scholar
  26. Hausen K, Wolburg-Buchholz K, Ribi WA (1980) The synaptic organization of visual interneurons in the lobula complex of flies. Cell Tissue Res 208:371–387Google Scholar
  27. Heisenberg M, Wonneberger R, Wolf R (1978) Optomotor blind H31 — aDrosophila mutant of the lobula plate giant neurons. J Comp Physiol 124:287–296Google Scholar
  28. Hengstenberg R (1977) Spike responses of ‘non-spiking’ visual interneurones. Nature 270:338–340Google Scholar
  29. Hengstenberg R, Hengstenberg B (1980) In: Strausfeld NJ, Miller TW (eds) Experimental entomology, vol I, Neuroanatomical techniques. Springer, Berlin Heidelberg New York, pp 307–324Google Scholar
  30. Kirschfeld K (1979) The visual system of the fly: physiological optics and functional anatomy as related to behaviour. In: Schmitt FO, Worden FG (eds) The neurosciences fourth study program. MIT Press, Cambridge, MA, London, pp 297–310Google Scholar
  31. Krieghoff D (1979) Einfluß des extra- und intrazellulären Ionenmilieus auf die lichtinduzierte Reizantwort von Photorezeptoren. Diplomarbeit, Universität BochumGoogle Scholar
  32. Mountcastle VB (1968) Medical physiology, vol II. Mosby, St. Louis, MO, pp 1070–1071Google Scholar
  33. Pierantoni R (1975) An observation of the giant fibre posterior optic tract in the fly. In: Drischel VH, Dettmar P (eds) Biokybernetik, Bd V. IV. Int Symp “Biokybernetik” (Leipzig 1973). Fischer, Jena, pp 157–163Google Scholar
  34. Pierantoni R (1976) A look into the cockpit of the fly. The architecture of the lobula plate. Cell Tissue Res 171:101–122Google Scholar
  35. Preissler M (1974) Struktur des inneren Chiasma im Sehsystem der FliegeMusca domestica. Diplomarbeit, Universität TübingenGoogle Scholar
  36. Reichardt W (1973) Musterinduzierte Flugorientierung. Verhaltensversuche an der FliegeMusca domestica. Naturwissenschaften 60:122–138Google Scholar
  37. Rivera M, Langer H (1978) Effect of light on ATPases in eyes and brain of the blowfly,Calliphora. J Comp Physiol 123:245–251Google Scholar
  38. Strausfeld NJ (1976a) Atlas of an insect brain. Springer, Berlin Heidelberg New YorkGoogle Scholar
  39. Strausfeld NJ (1976b) Mosaic organization, layers, and visual pathways in the insect brain. In: Zettler F, Weiler R (eds) Neural principles in vision. Springer, Berlin Heidelberg New York, pp 245–279Google Scholar
  40. Strausfeld NJ, Nässel DR (1980) Neuroarchitecture of brain regions that subserve the compound eyes of crustacea and insects. In: Handbook of sensory physiology, vol VII/6B. Autrum H (ed) Springer, Berlin Heidelberg New York, pp 1–132Google Scholar
  41. Strausfeld NJ, Obermayer M (1976) Transneuronal migration of cobalt and nickel in insect central nervous system: I. Diffusion rates and movement into functional classes of neurons. J Comp Physiol 110:1–12Google Scholar
  42. Tyrer NM, Bell EM (1974) The intensification of cobalt-filled neurone profiles using a modification of TIMM's sulphide-silver method. Brain Res 73:151–156Google Scholar
  43. Wehrhahn C (1978) Flight torque and lift responses of the housefly (Musca domestica) to a single stripe moving in different parts of the visual field. Biol Cybern 29:237–247Google Scholar
  44. Wehrhahn C (1979) Sex-specific differences in the chasing behaviour of houseflies (Musca). Biol Cybern 32:239–241Google Scholar
  45. Wehrhahn C, Reichardt W (1975) Visually induced height orientation of the flyMusca domestica. Biol Cybern 20:37–50Google Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • Hendrik Eckert
    • 1
  1. 1.Department of Animal PhysiologyRuhr-University BochumBochum 1Federal Republic of Germany

Personalised recommendations