Summary
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1.
A glass microelectrode was inserted into the optic lobes of fleshflies (Boettcherisca peregrina) and discharges responding to the movement of a spot of light were recorded.
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2.
Units responding to moving spot were classified into four types: non-directional, one directional, semi-integrative and integrative types. In addition, there was an “alerting” unit which discharged phasically to movement of a spot in any direction and adapted quickly, and an “inhibitory” unit in which discharges were inhibited by movement of a spot in any direction although a preferred direction was seen slightly.
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3.
Units of the non-directional type with relatively narrow receptive fields were found in the medulla only, while those with wide fields were in the lobula and the pathway to the central brain.
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4.
Units of the one directional type, which discharge to a preferred direction, were found in the region of the medulla to the lobula regardless of the size of the receptive field.
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5.
Units of the semi-integrative type, which possess a receptive field apparently formed by the combination of two or more fields of the one directional type and sometimes discharge dominantly to vertical movement at the front along the head axis, were found in all regions of the medulla to such central parts as the optic peduncle.
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6.
Units of the integrative type, which respond to such complex, but continuous movement as a circular motion of objects, were found in the central region from the lobula to the pathways to the brain.
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7.
Four types of relationships were found between the speed of the moving spot and the discharge rate: a, the discharge rate increased proportionally to the logarithm of the increase of the speed; b, the discharge rate was not altered by the speed changes; c, the discharge rate became maximal at a particular speed; d, the discharge rate was decreased or inhibited with increase of the speed.
Type a was mainly seen in units of the one directional type with a wide receptive field and in units of the semi-integrative type, and was distributed over the region from the medulla to the lobula. Type b was found in units of the non-directional type with a narrow receptive field, and was situated in the medulla only. Type c was related with units of the directional and integrative types, and located in the central region of the optic lobes. Type d, seen in only few number, was found in the pathway to the central brain.
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8.
Orderly arrangement of the units, which suggests a neural mechanism for directional selectivity, was electrophysiologically observed.
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9.
It is concluded that the analytical processing of the direction and speed of movement is conducted in the region of the medulla to the lobula, and that the neural integration is performed in the central part of the optic lobes, the lobula and the pathway to the central brain.
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References
Arden, G. B.: Complex receptive fields and responses to moving objects in cells of the rabbit's lateral geniculate body. J. Physiol. (Lond.) 166, 468–488 (1763).
Barlow, H. B., Hill, R. M.: Selective sensitivity to direction of motion in ganglion cells of the rabbit's retina. Science 139, 412–414 (1963).
—, Levick, W. R.: Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J. Physiol. (Lond.) 173, 377–407 (1964).
—, Levick, W. R.: The mechanism of directionally selective units in rabbit's retina. J. Physiol. (Lond.) 178, 477–504 (1965).
Baumgartner, G., Brown, J. L., Schulz, A.: Visual motion detection in the cat. Science 146, 1070–1071 (1964).
Bishop, L. G., Keehn, D. G.: Neural correlates of the optomotor response in the fly. Kybernetik 3, 288–295 (1967).
—: McCann, G. D.: Motion detection by interneurons of optic lobes and brain of the flies Calliphora phaenicia and Musca domestica. J. Neurophysiol. 31, 509–525 (1968).
Braitenberg, V.: Patterns of projection in the visual system of the fly. I. Retina-lamina projections. Exp. Brain Res. 3, 271–298 (1967).
Burtt, E. T., Catton, W. T.: Visual perception of movement in the locust. J. Physiol. (Lond.) 125, 566–580 (1954).
—: Electrical responses to visual stimulation in the optic lobe of the locust and certain other insects. J. Physiol. (Lond.) 133, 68–88 (1956).
—: Transmission of visual responses in the nervous system of the locust. J. Physiol. (Lond.) 146, 492–515 (1959).
—: The properties of single-unit discharges in the optic lobe of the locust. J. Physiol. (Lond.) 154, 479–490 (1960).
—: Perception by locusts of rotated patterns. Science 151, 224 (1966).
—: Resolution of the locust eye measured by rotation of radial striped patterns Proc. roy. Soc. B 173, 513–529 (1969).
Collett, A. D., Blest, J.: Binocular directionaliy sensitive neurones, possibly involved in optomotor response of locusts. Nature (Lond.) 212, 1330–1333 (1966).
Fermi, G. von, Reichardt, W.: Optomotorische Reaktionen der Fliege Musca domestica. Kybernetik 2, 15–28 (1963).
Finkelstein, D., Grüsser, O. J.: Frog retina: detection of movement. Science 150, 1050–1051 (1965).
Horridge, G. A.: Multimodal interneurones of locust optic lobe. Nature (Lond.) 204, 499–501 (1964).
Hubel, D. H., Wiesel, T. N.: Receptive fields of single neurones in the cat's striate cortex. J. Physiol. (Lond.) 148, 574–591 (1959).
Kozak, W., Rodieck, R. W., Bishop, P. O.: Responses of single units in lateral geniculate nucleus of cat to moving visual patterns. J. Neurophysiol. 28, 19–47 (1965).
Lettvin, J. Y., Maturana, H. R., McCulloch, W. S., Pitts, W. H.: What the frog's eye tells the frog's brain. Proc. IEEE. 47, 1940–1951 (1959).
Maturana, H. R., Frenk, S.: Directional movement and horizontal edge detectors in pigeon retina. Science 142, 977–979 (1963).
McCann, G. D., Dill, J. C.: Fundamental properties of intensity, form, and motion perception in the visual nervous systems of Calliphora phaenicia and Musca domestica. J. gen. Physiol. 53, 385–413 (1969).
Mimura, K.: Integration and analysis of movement information by the visual system of flies. Nature (Lond.) 226, 964–966 (1970).
Mulloney, B.: Interneurons in the central nervous system of flies and the start of flight. Z. vergl. Physiol. 64, 243–253 (1969).
Norton, A. L., Spekreijse, H., Wagner, H. G., Wolbarsht, M. L.: Response to directional stimuli in retinal preganglionic units. J. Physiol. (Lond.) 206, 93–107 (1970).
Palka, J.: Discrimination between movements of eye and object by visual interneurones of crickets. J. exp. Biol. 50, 723–732 (1969).
Satija, R. C.: A histological study of the brain and thoracic nerve cord of Calliphora erythrocephala with special reference to the descending nervous pathways. Res. Bull. Panjab Univ. 142, 81–96 (1958).
Swihart, S. L.: Colour vision and the physiology of the superposition eye of a butterfly (Hesperiidae). J. Insect Physiol. 15, 1347–1365 (1969).
Waterman, T. H., Wiersma, C. A. G., Bush, B. M. H.: Afferent visual responses in the optic nerve of the crab Podophthalmus. J. cell. comp. Physiol. 63, 135–155 (1964).
Wiersma, C. A. G., Bush, B. M. H., Waterman, T. H.: Efferent visual responses of contralateral origin in the optic nerve of the crab Podophthalmus. J. cell. comp. Physiol. 64, 309–326 (1964).
—, Oberjat, T.: The selective responsiveness of various crayfish oculomotor fibers to sensory stimuli. Comp. Biochem. Physiol. 26, 1–16 (1968).
—, Yamaguchi, T.: The neuronal components of the optic nerve of the crayfish as studied by single unit analysis. J. comp. Neurol. 128, 333–358 (1966).
—: The integration of visual stimuli in the rock lobster. Vision Res. 7, 197–204 (1967).
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I wish to express my appreciation to Prof. M. Kuwabara and Dr. H. Tateda (Department of Biology, Faculty of Sciences, Kyushu University) for their support and encouragement in this work. Thanks are due to Drs. Y. Toh and H. Kondo of the same Department for their help in breeding the fly. I am grateful to the above mentioned Department and also to the Department of Physiology, Nagasaki University School of Medicine (Prof. K. Sato) for their help in the histological procedures.
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Mimura, K. Movement discrimination by the visual system of flies. Z. Vergl. Physiol. 73, 105–138 (1971). https://doi.org/10.1007/BF00304129
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DOI: https://doi.org/10.1007/BF00304129