Predictive coding: a fresh view of inhibition in the retina

The Royal Society - Tập 216 Số 1205 - Trang 427-459 - 1982
Mandyam V. Srinivasan1, Simon B. Laughlin2, Andreas Dubs2
1Departments of Neurobiology and Applied Mathematics, Australian National University, P. O. Box 475, Canberra City, A. C. T., 2601, Australia
2Departments of Neurobiology, Australian National University, P. O. Box 475, Canberra City, A. C. T., 2601, Australia

Tóm tắt

Interneurons exhibiting centre-surround antagonism within their recep­tive fields are commonly found in peripheral visual pathways. We propose that this organization enables the visual system to encode spatial detail in a manner that minimizes the deleterious effects of intrinsic noise, by exploiting the spatial correlation that exists within natural scenes. The antagonistic surround takes a weighted mean of the signals in neighbouring receptors to generate a statistical prediction of the signal at the centre. The predicted value is subtracted from the actual centre signal, thus minimizing the range of outputs transmitted by the centre. In this way the entire dynamic range of the interneuron can be devoted to encoding a small range of intensities, thus rendering fine detail detectable against intrinsic noise injected at later stages in processing. This predictive encoding scheme also reduces spatial redundancy, thereby enabling the array of interneurons to transmit a larger number of distinguishable images, taking into account the expected structure of the visual world. The profile of the required inhibitory field is derived from statistical estimation theory. This profile depends strongly upon the signal: noise ratio and weakly upon the extent of lateral spatial correlation. The receptive fields that are quantitatively predicted by the theory resemble those of X-type retinal ganglion cells and show that the inhibitory surround should become weaker and more diffuse at low intensities. The latter property is unequivocally demonstrated in the first-order interneurons of the fly’s compound eye. The theory is extended to the time domain to account for the phasic responses of fly interneurons. These comparisons suggest that, in the early stages of processing, the visual system is concerned primarily with coding the visual image to protect against subsequent intrinsic noise, rather than with reconstructing the scene or extracting specific features from it. The treatment emphasizes that a neuron’s dynamic range should be matched to both its receptive field and the statistical properties of the visual pattern expected within this field. Finally, the analysis is synthetic because it is an extension of the background suppression hypothesis (Barlow & Levick 1976), satisfies the redundancy reduction hypothesis (Barlow 1961 a, b) and is equivalent to deblurring under certain conditions (Ratliff 1965).

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Tài liệu tham khảo

10.1037/h0054663

Barlow H. B. 1961a Possible principles underlying the transform ation of sensory messages. In Sensory communication (ed. W. A. Rosenblith) pp. 217-234. Cambridge M assachusetts: M.I.T. Press.

Barlow H. B. 19616 Three points about lateral inhibition. In Sensory communication (ed. W. A. Rosenblith) pp. 782-786. Cambridge M assachusetts: M.I.T. Press.

Barlow H. B. 1961c The coding of sensory messages. In Current problems in animal behaviour (ed. W. H. Thorpe & O. L. Zangwill) pp. 331-360. Cambridge University Press.

10.1098/rspb.1981.0022

10.1113/jphysiol.1957.sp005817

Barlow H. B., 1976, Threshold setting by the surround of cat retinal ganglion cells. J.Physiol, Lond., 259, 737

10.1007/BF00235589

Brodie S. E., 1978, The spatiotem poral transfer function of the Lim ulus lateral eye. J. gen, Physiol., 72, 167

10.1113/jphysiol.1966.sp008056

10.1113/jphysiol.1968.sp008574

Collett T., 1975, Visual control of flight behaviour in the hoverfly, Syritta pipiens L. J. comp, Physiol., 99, 1

10.1016/0042-6989(74)90118-7

Dubs A., 1982, The spatial integration of signals in the retina and lamina of the fly compound eye under different conditions of Iuminance. J. comp, Physiol., 146, 321

10.1113/jphysiol.1981.sp013827

10.1113/jphysiol.1966.sp008107

10.1113/jphysiol.1973.sp010308

French A. S., 1978, The transmission of information by first and second order neurons in the fly visual system. J. comp, Physiol., 126, 87

10.1113/jphysiol.1975.sp011162

Gonzalez R. C. & W intz P. 1977 Digital image processing. London: Addison-Wesley.

Grenander U. & Szego G. 1958 Toeplitzforms and their application. Berkeley and Los Angeles: University of California Press.

Hardie R. C., 1979, Electrophysiological analysis of fly retina. I. Comparative properties of R 1-6 and R7 and 8. J. comp, Physiol., 129, 19

Harrison C. W. 1952 Experim ents with linear prediction in television. Bell Syst. tech. J. 31 764-783.

Hartline H. K. & Ratliff F. 1972 Inhibitory interactions in the retina of Limulus. In Handbook of sensory physiology vol. 7 (2) (ed. M. G. F. Fuortes) pp. 381-447. Berlin: Springer.

Howard J., 1981, The temporal resolving power of the photoreceptors of Locusta migratoria. J. comp, Physiol., 144, 61

Howard J. Dubs A. & Payne R. 1982 The dynamics of phototransduction in insects - a com parative study. J. comp. Physiol. (Submitted.)

Hughes A. 1977 The topography of vision in mammals of contrasting life style: com parative optics and retinal organisation. In pp. 613-756. Berlin: Springer.

Handbook of sensory ph vol. 7 (5) (ed. F. Crescitelli)

Hughes A., 1981, Cat retina and the sampling theorem : the relation of transient and sustained brisk-unit cut-off frequency to a and (3 mode cell density, Brain Res., 42, 196

10.1364/JOSA.51.000422

10.1007/BF00235588

Kretzmer E. R. 1952 Statistics of television signals. Bell Syst. tech. J. 31 751-763.

10.1152/jn.1953.16.1.37

Laughlin S. B. 1981a Neural principles in the peripheral visual systems of invertebrates. In Handbook of sensory physiology vol. 7 (6 B) (ed. H. Autrum) pp. 133-280. Berlin: Springer.

Laughlin S. B. 19816 A simple coding procedure enhances a neuron's information capacity. Z. Naturf. 36c 910-912.

Laughlin S. B., 1978, Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J. comp, Physiol., 128, 319

10.1113/jphysiol.1975.sp010893

Mach E., 1865, Uber die Wirkung der raumlichen Vertheileng des Lichtreizes auf die Netzhaut, Sber. Akad. WTss. Wien (II), 52, 303

10.1111/j.2044-8295.1956.tb00559.x

10.1007/BF00337645

10.1098/rspb.1980.0020

Miller W. H. 1979 Ocular optical filtering. In Handbook of sensory physiology vol. 7 (6A) (ed. H. Autrum) pp. 69-143. Berlin: Springer.

Mimura K., 1976, Some spatial properties in the first optic ganglion of the fly. J. comp, Physiol., 105, 65

Norman R. A., 1974, Control of retinal sensitivity. 1. Light and dark-adaptation of vertebrate rods and cones. J. gen, Physiol., 63, 37

Oliver B. M. 1952 Efficient coding. Bell Syst. tech. J. 31 724-750.

Papoulis A. 1965 Probability random variables and stochastic processes. Tokyo: McGraw-Hill Kogakusha.

Purple R. L., 1965, Interaction of excitation and inhibition in the eccentric cell in the eye of Limulus. Cold Spring Harb. Symp. quant, Biol., 30, 529

Ratliff F. 1965 Mach bands: quantitative studies on neural networks in the retina. San Francisco: Holden-Day.

10.1364/JOSA.56.001141

10.1152/jn.1965.28.5.819

Rosenfeld A. & Kak A. C. 1976 Digital picture processing. New York: Academic Press.

Shaw S. 1978 Signal transmission by graded slow potentials in the arthropod peripheral visual system. In The neurosciences: fourth study program (ed. F. O. Schm itt & F. G. Worden) pp. 275-295. Cambridge Massachusetts: M.I.T. Press.

Snyder A. W. 1979 Physics of vision in compound eyes. In Handbook of sensory physiology vol. 7 (6 A) (ed. H. Autrum) pp. 225-313. Berlin: Springer.

10.1007/BF00337446

10.1016/0042-6989(75)90029-2

Srinivasan M. V., 1980, Spatial processing of visual information in the movement-detecting pathw ay of the fly. J. comp, Physiol., 140, 1

Wehner R. 1981 Spatial vision in arthropods. In Handbook of sensory physiology vol. 7 (6 C) (ed. H. Autrum) pp. 287-616. Berlin and New York: Springer.

10.1152/jn.1971.34.2.228

Werblin F. S. 1974 Control of retinal sensitivity. II. Lateral interactions at the outer plexiform layer. J. gen.Physiol. 63 62-87.

10.1016/0042-6989(79)90117-2

Zettler F., 1969, Die Abhangigkeit des U bertragungsverhaltens von Frequenz und Adaptationszustand, gemessen am einzelnen Lichtrezeptor von Calliphora erythrocephala. vergl, Physiol., 64, 432

Zettler F., 1972, Lateral inhibition in an insect eye. Z. vergl, Physiol., 76, 233