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Mechanisms of early visual processing in the medulla of the locust optic lobe: How self-inhibition, spatial-pooling, and signal rectification contribute to the properties of transient cells

Published online by Cambridge University Press:  02 June 2009

D. Osorio
D. Osorio
Affiliation:
Centre for Visual Sciences, Research School of Biological Sciences, Australian National University, ACT 2601, Australia
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Abstract

In the arthropod medulla, which is the second ganglion on the afferent visual pathway, a column of about 40 cells represents each point in space (i.e. compound eye facet). Some stages of visual processing underlying the responses of one class of cells in the locust medulla have been identified. These transient cells give very similar responses to intensity increments and decrements, and also to pulses and steps; there is no spontaneous activity and a stimulus causes one or two spikes to fire at fixed latencies. Movement, however, produces a prolonged spike discharge by successive excitation of subunits within the receptive field.

One of the main features of the transient cells' responses is a self-inhibition which attenuates responses to successive stimuli at one point. This inhibition is restricted to the outputs of single receptor (rhabdom), it decays after about 100 ms, and is polarity sensitive so that stimuli of one polarity (e.g. dimming) do not inhibit responses to stimuli of the opposite polarity (e.g. brightening). The inhibition effectively alters the contrast threshold of the cells, because after adaptation with stimuli of one contrast, a modest (<20%) increase in contrast is sufficient to elicit an unadapted response. Transient cells are not directionally selective and there are no local spatio-temporal interactions of the kind necessary for directional selectivity. But, by analogy with the directional veto in directionally selective cells in the rabbit retina (Barlow & Levick, 1965), self-inhibition is suggested as a mechanism of non-directional motion detection. After the inhibition, there is some spatial pooling of signals which is followed by rectification. The transient cells' spiking outputs could abstract a refined subset of visual information which may encode the presence, but not the direction, amplitude, or polarity of moving object borders.

Keywords

Transient cellsSustaining cellsVisual processingLocust (Locusta migratoria)Optic lobeArthropodsPhotoreceptors
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 4 , October 1991 , pp. 345 - 355
Copyright
Copyright © Cambridge University Press 1991

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References

Barlow, H.B. & Levick, W.R. (1965). The mechanism of directionally selective units in the rabbit's retina. Journal of Physiology 178, 477–504.CrossRefGoogle ScholarPubMed
Borst, A. & Egelhaaf, M. (1989). Principles of visual motion detection. Trends in Neurosciences 12, 297–306.CrossRefGoogle ScholarPubMed
Burtt, E.T. & Catton, W.T. (1956). Electrical responses to visual stimulation in the optic lobes of locusts and certain other insects. Journal of Physiology 133, 492–515.CrossRefGoogle ScholarPubMed
DeVoe, R.D. & Ockleford, E.M. (1976). Intracellular responses from cells of the medulla of the fly Calliphora erythrocephala. Biological Cybernetics 23, 13–24.CrossRefGoogle ScholarPubMed
Dubs, A. (1982). The spatial integration of signals in the retina and lamina of the fly compound eye under different conditions of luminance. Journal of Comparative Physiology A 146, 321–334.CrossRefGoogle Scholar
Egelhaaf, M., Borst, A. & Reichardt, W. (1989). Computational structure of a biological motion detection system as revealed by local detector analysis in the fly's nervous system. Journal of the Optical Society of America A 6, 1070–1087.CrossRefGoogle ScholarPubMed
Fischbach, K.-F. & Dittrich, A.P.M. (1989). The optic lobe of Drosophila melanogaster I. A Golgi analysis of wild-type structure. Cell and Tissue Research 258, 441–475.CrossRefGoogle Scholar
Franceschini, N., Riehle, A. & Nestour, A.le (1989). Directionally selective motion detection by insect neurons. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 360–390. Berlin: Springer.CrossRefGoogle Scholar
Hausen, K. & Egelhaaf, M. (1989). Neural mechanisms of visual course control in insects. In Facets of Vision, ed. Stavenga, D.G. & Hardie, R.C., pp. 391–424. Berlin: Springer.CrossRefGoogle Scholar
Hochstein, S. & Shapley, R.M. (1976). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology 262, 265–284.CrossRefGoogle ScholarPubMed
Honegger, H.-W. (1978). Sustained and transient responding units in the medulla of the cricket Gryllus campestris. Journal of Comparative Physiology 125, 259–266.CrossRefGoogle Scholar
zHorn, G. & Rowell, C.H.F. (1968). Medium and long term changes in the behaviour of visual neurones in the tritocerebrum of locusts. Journal of Experimental Biology 49, 143–169.CrossRefGoogle Scholar
Horridge, G.A. (1978). The separation of visual axes in apposition compound eyes. Philosophical Transactions of the Royal Society A (London) 285, 1–59.Google Scholar
James, A.C. (1991). Nonlinear transformations in the fly lamina. In Nonlinear Vision, ed. Pinter, R.B. & Nabet, B., CRC Press (in press).Google Scholar
Kien, J. (1974). Sensory integration in the locust optomotor system. II Direction selective neurons in the circumoesophageal connectives and the optic lobe. Vision Research 14, 1255–1268.CrossRefGoogle ScholarPubMed
Levick, W.R. & Thibos, L.N. (1983). Receptive fields of cat ganglion cells: classification and construction. In Progress in Retinal Research, Vol. 2, ed. Osborne, N. & Chader, G., pp. 267–319. Oxford, New York: Pergamon.Google Scholar
O'Shea, M. & Rowell, C.H.F. (1976). The neuronal basis of a sensory analyser, the acridid movement detector system II. Response decrement, convergence, and the nature of the excitatory afferents to the fan-like dendrites of the LGMD. Journal of Experimental Biology 65, 289–308.CrossRefGoogle Scholar
Osorio, D. (1968a). Directionally selective cells in the locust medulla. Journal of Comparative Physiology A 159, 841–847.CrossRefGoogle Scholar
Osorio, D. (1986b). Ultraviolet sensitivity and spectral opponency in the locust. Journal of Experimental Biology 122, 193–208.CrossRefGoogle Scholar
Osorio, D. (1987a). The temporal properties of non-linear transient cells in the locust medulla. Journal of Comparative Physiology A 161, 431–440.CrossRefGoogle Scholar
Osorio, D. (1987b). Temporal and spectral properties of sustaining cells in the medulla of the locust. Journal of Comparative Physiology A 161, 441–448.CrossRefGoogle Scholar
Osorio, D., Snyder, A.W. & Srinivasan, M.V. (1987). Bi-partitioning and boundary detection in natural scenes. Spatial Vision 2, 191–198.Google ScholarPubMed
Palka, J. (1967). An inhibitory process influencing visual responses to a fibre of the ventral nerve chord of locusts. Journal of Insect Physiology 13, 235–248.CrossRefGoogle Scholar
Pinter, R.B. (1972). Frequency and time domain properties of retinular cells of the desert locust (Schistocerca gregaria) and the house cricket (Acheta domesticus). Journal of Comparative Physiology 77, 383–397.CrossRefGoogle Scholar
Ratliff, F. (1965). Mach Bands–Quantitative Studies of Inhibition in the Retina. San Francisco, California: Holden-Day.Google Scholar
Reichardt, W. (1969). Movement perception in insects. In Processing of Optical Data by Organisms and by Machines, ed. Reichardt, W., pp. 465–493. New York, London: Academic Press.Google Scholar
Rind, F.C. (1987). Non-directional, movement sensitive neurones of the locust optic lobe. Journal of Comparative Physiology A 161, 477–494.CrossRefGoogle Scholar
Rind, F.C. (1990). Identification of directionally selective motion-detecting neurones in the locust lobula and their synaptic connections with an identified descending neurone. Journal of Experimental Biology 149, 21–43.CrossRefGoogle Scholar
Rowell, C.H.F. (1971). The orthopteran descending movement detector (DMD) neurons: a characterisation and review. Zeitschrift fuer Vergleichende Physiologie 73, 167–194.CrossRefGoogle Scholar
Rowell, C.H.F. & Horn, G. (1968). Dishabituation and arousal in the responses of single nerve cells in an insect brain. Journal of Experimental Biology 49, 171–184.CrossRefGoogle Scholar
Rowell, C.H.F. & O'Shea, M. (1976). The neuronal basis of a sensory analyser, the acridid movement detector system. III. Control of response amplitude by tonic lateral inhibition. Journal of Experimental Biology 65, 617–625.CrossRefGoogle Scholar
Rowell, C.H.F., O'Shea, M. & Williams, J.L.D. (1977). The neuronal basis of a sensory analyser, the acridid movement detector system. I. The preference for small field stimuli Journal of Experimental Biology 68, 157–185.CrossRefGoogle Scholar
Strausfeld, N.J. (1976). Atlas of an Insect Brain. Berlin, Heidelberg, New York: Springer.CrossRefGoogle Scholar
Torre, V. & Poggio, T. (1978). A synaptic mechanism possibly underlying directional selectivity to motion. Proceedings of the Royal Society B (London) 202, 409–416.Google Scholar
Victor, J.D. & Shapley, R.M. (1979). The nonlinear pathway of Y ganglion cells in the cat retina. Journal of General Physiology 74, 671–689.CrossRefGoogle ScholarPubMed
Wiersma, C.A.G., Roach, J.L.M. & Glantz, R.M. (1982). Neural integration in the optic system. In The Biology of Crustacea, Vol. 4 ed. Atwood, H. & Sandeman, D.C., pp. 1–31. New York: Academic Press.Google Scholar
Zaretsky, M. & Rowell, C.H. (1979). Saccadic suppression by corollary discharge in the locust. Nature 280, 583–585.CrossRefGoogle ScholarPubMed