Visual control of orientation behaviour in the fly: Part II. Towards the underlying neural interactions

Visual information processing in the nervous system of flies begins with a large array of photoreceptors, which transduce a light intensity pattern, and culminates in a behavioural response that depends on that pattern. In the previous paper we have given a quantitative description of visual control of flight orientation in the fly. This description can account for fixation, tracking and some instances of spontaneous pattern preference behaviour. The phenomenological theory outlines the basic logical organization of the visual control system of the fly. It requires the neural network between the receptors and the flight muscles to perform two main computations on the visual input. One computation extracts movement information (the term r (ψ)ψ b of the phenomenological equation). The other provides position information (the term D (ψ)).

[1]  E. Hille.  Functional Analysis And Semi-Groups , 1948 .

[2]  N. Wax,et al.  Selected Papers on Noise and Stochastic Processes , 1955 .

[3]  B. Hassenstein,et al.  Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus , 1956 .

[4]  W. Reichardt.  Autokorrelations-Auswertung als Funktionsprinzip des Zentralnervensystems , 1957 .

[5]  D. Varjú.  Optomotorische Reaktionen auf die Bewegung periodischer Helligkeitsmuster , 1959 .

[6]  W. Pitts,et al.  What the Frog's Eye Tells the Frog's Brain , 1959, Proceedings of the IRE.

[7]  B. Hassenstein.  Optokinetische Wirksamkeit bewegter periodischer Muster (Nach Messungen am Rüsselkäfer Chlorophanus viridis) , 1959 .

[8]  W. Reichardt,et al.  Übertragungseigenschaften im Auswertesystem für das Bewegungssehen , 1959 .

[9]  G. Zames.  Nonlinear operators of system analysis , 1960 .

[10]  J. Thorson.  Dynamics of Motion Perception in the Desert Locust , 1964, Science.

[11]  W. Reichardt,et al.  Quantum sensitivity of light receptors in the compound eye of the fly Musca. , 1965, Cold Spring Harbor symposia on quantitative biology.

[12]  Hubert M. James,et al.  Theory of Servomechanisms , 1965 .

[13]  Y. W. Lee,et al.  Measurement of the Wiener Kernels of a Non-linear System by Cross-correlation† , 1965 .

[14]  G. D. Mccann,et al.  Optomotor response studies of insect vision , 1965, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[15]  E. Wong,et al.  ON THE RELATION BETWEEN ORDINARY AND STOCHASTIC DIFFERENTIAL EQUATIONS , 1965 .

[16]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[17]  A. Skorokhod,et al.  Studies in the theory of random processes , 1966 .

[18]  R. Wyman.  Multistable firing patterns among several neurons. , 1966, Journal of neurophysiology.

[19]  T. Collett,et al.  Binocular, Directionally Selective Neurones, Possibly Involved in the Optomotor Response of Insects , 1966, Nature.

[20]  A. L. I︠A︡rbus.  Eye Movements and Vision , 1967 .

[21]  W. Nachtigall,et al.  Neuro-muscular control of dipteran flight. , 1967, The Journal of experimental biology.

[22]  C. R. Michael.  Receptive fields of single optic nerve fibers in a mammal with an all-cone retina. II: directionally selective units. , 1968, Journal of neurophysiology.

[23]  G. Fravi.  Prazipitierende leber-autoantikorper bei der maus. , 1968 .

[24]  J. Robson,et al.  Application of fourier analysis to the visibility of gratings , 1968, The Journal of physiology.

[25]  L. Kaufman,et al.  “Center-of-gravity” Tendencies for fixations and flow patterns , 1969 .

[26]  G. Marchesini,et al.  On the evaluation of the response of nonlinear systems by functional series expansion of forced and free responses , 1969 .

[27]  G. D. Mccann,et al.  Fundamental Properties of Intensity, Form, and Motion Perception in the Visual Nervous Systems of Calliphora phaenicia and Musca domestica , 1969, The Journal of general physiology.

[28]  D. Fender,et al.  Nonlinearities of the human oculomotor system: gain. , 1969, Vision research.

[29]  N. Sancho.  Moment equations of a stochastic system with two different random parameters , 1969 .

[30]  V. Montero,et al.  Direction of movement as the significant stimulus parameter for some lateral geniculate cells in the rat. , 1969, Vision research.

[31]  Werner Reichardt,et al.  Processing of optical data by organisms and by machines , 1969 .

[32]  T. Collett.  Centripetal and centrifugal visual cells in medulla of the insect optic lobe. , 1970, Journal of neurophysiology.

[33]  G. C. Quarton,et al.  The Neurosciences;: Second study program , 1970 .

[34]  E. Bedrosian,et al.  The output properties of Volterra systems (nonlinear systems with memory) driven by harmonic and Gaussian inputs , 1971 .

[35]  THOMAS COLLETT,et al.  Visual Neurones for Tracking Moving Targets , 1971, Nature.

[36]  H. Haken,et al.  Generalized thermodynamic potential for Markoff systems in detailed balance and far from thermal equilibrium , 1971 .

[37]  D. Arnett.  Receptive Field Organization of Units in the First Optic Ganglion of Diptera , 1971, Science.

[38]  Bernard D. Coleman,et al.  A mathematical theory of lateral sensory inhibition , 1971 .

[39]  Boschek Cb.  On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. , 1971 .

[40]  B. D. Coleman.  On retardation theorems , 1971 .

[41]  B. Julesz.  Foundations of Cyclopean Perception , 1971 .

[42]  I. Prigogine,et al.  Fluctuations in nonequilibrium systems. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[43]  A. Halme,et al.  Polynomial operators in non-linear systems theory , 1971 .

[44]  V. Braitenberg.  Periodic structures and structural gradients in the visual ganglia of the fly , 1972 .

[45]  K. Kirschfeld.  The visual system of Musca: Studies on optics, structure and function , 1972 .

[46]  George W. Stroke,et al.  Optical computing , 1972, IEEE Spectrum.

[47]  W M Smith.  Feedback: Real-Time Delayed Vision of One's Own Tracking Behavior , 1972, Science.

[48]  William C. Lindsey,et al.  SYNCHRONIZATION SYSTEMS in Communication and Control , 1972 .

[49]  John Palka,et al.  Moving Movement Detectors , 1972 .

[50]  Karl Georg Götz.  Spontaneous preferences of visual objects in Drosophila , 1972 .

[51]  K G Götz,et al.  Principles of optomotor reactions in insects. , 1972, Bibliotheca ophthalmologica : supplementa ad ophthalmologica.

[52]  E. Bizzi,et al.  Central programming and peripheral feedback during eye-head coordination in monkeys. , 1972, Bibliotheca ophthalmologica : supplementa ad ophthalmologica.

[53]  Gerrits Hj,et al.  Eye movements necessary for continuous perception during stabilization of retinal images. , 1972 .

[54]  N. Strausfeld,et al.  Columns and Layers in the Second Synaptic Region of the Fly’s Visual System: The Case for Two Superimposed Neuronal Architectures , 1972 .

[55]  R. Hengstenberg.  The Effect of Pattern Movement on the Impulse Activity of the Cervical Connective of Drosophila melanogaster , 1973, Zeitschrift fur Naturforschung. Teil C: Biochemie, Biophysik, Biologie, Virologie.

[56]  S. Benzer.  Genetic dissection of behavior. , 1973, Scientific American.

[57]  N. Strausfeld,et al.  The L4 monopolar neurone: a substrate for lateral interaction in the visual system of the fly Musca domestica (L.). , 1973, Brain research.

[58]  N. Strausfeld,et al.  Synaptic connections of intrinsic cells and basket arborizations in the external plexiform layer of the fly's eye. , 1973, Brain research.

[59]  A. A. Skavenski,et al.  Miniature eye movement. , 1973, Science.

[60]  M. F. LAND,et al.  Head Movement of Flies during Visually Guided Flight , 1973, Nature.

[61]  L. Maffei,et al.  The visual cortex as a spatial frequency analyser. , 1973, Vision research.

[62]  F. Newell.  Information Processing in the Visual Systems of Arthropods , 1973 .

[63]  K. Kirschfeld.  DAS NEURALE SUPERPOSITIONSAUGE , 1973 .

[64]  S. Laughlin.  Neural integration in the first optic neuropile of dragonflies , 1973 .

[65]  R. Phelps.  Effects of interactions of two moving lines on single unit responses in the cat's visual cortex. , 1974, Vision research.

[66]  K. Kirschfeld,et al.  Lateral Inhibition in the Com pound Eye of the Fly, Musca , 1974, Zeitschrift fur Naturforschung. Section C, Biosciences.

[67]  F. G. Worden,et al.  The neurosciences : third study program , 1974 .

[68]  C. Wehrhahn.  Verhaltensstudie zur visuallen Höhenorientierung der Fliege Musca domestica , 1974 .

[69]  R. Thom.  Stabilité structurelle et morphogenèse , 1974 .

[70]  K. Naka,et al.  Identification of multi-input biological systems. , 1974, IEEE transactions on bio-medical engineering.

[71]  Bernward Pick,et al.  Visual Flicker Induces Orientation Behaviour in the Fly Musca , 1974 .

[72]  V. Glezer,et al.  Studies on visual pattern recognition in man and animals. , 1974, Vision research.

[73]  G. D. Lange,et al.  A Nonlinearity in the Inhibitory Interactions in the Lateral Eye of Limulus , 1974, The Journal of general physiology.

[74]  F. Campbell,et al.  The effect of phase on the perception of compound gratings. , 1974, Vision research.

[75]  M. O'Shea,et al.  Protection from habituation by lateral inhibition , 1975, Nature.

[76]  B Julesz,et al.  Experiments in the visual perception of texture. , 1975, Scientific American.

[77]  S. Laughlin.  Receptor and Interneuron Light-adaptation in the Dragonfly Visual System , 1975, Zeitschrift fur Naturforschung. Section C, Biosciences.

[78]  T. Poggio,et al.  The Muller-Lyer figure and the fly , 1975, Science.

[79]  Yoshinori Uesaka.  Analog Perceptron: Its Decomposition and Order , 1975, Inf. Control..

[80]  W. Porter,et al.  On the analysis of feedback systems with a polynomic plant , 1975 .

[81]  D. Broadbent,et al.  Some experiments bearing on the hypothesis that the visual system analyses spatial patterns in independent bands of spatial frequency , 1975, Vision Research.

[82]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of striate cortical neurones , 1975, Nature.

[83]  Hh Bülthoff.  Nachweis einer Bewegungsillusion im visuellen System der Fruchtfliege Drosophila , 1975 .

[84]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[85]  K. Kirschfeld,et al.  Waveguide Mode Effects, Birefringence and Dichroism in Fly Photoreceptors , 1975 .

[86]  D. Varjú.  Stationary and dynamic responses during visual edge fixation by walking insects , 1975, Nature.

[87]  F. Zettler,et al.  Neural principles in vision , 1976 .

[88]  Michael A. Arbib,et al.  Foundations of system theory: multidecomposable systems☆ , 1976 .

[89]  N. Strausfeld.  Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.

[90]  C. WEHRHAHN,et al.  Real-time delayed tracking in flies , 1976, Nature.

[91]  W Reichardt,et al.  Nonlinear interactions underlying visual orientation behavior of the fly. , 1976, Cold Spring Harbor Symposia on Quantitative Biology.

[92]  Patrick Henry Winston,et al.  The psychology of computer vision , 1976, Pattern Recognit..

[93]  D Marr,et al.  Early processing of visual information. , 1976, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[94]  W. Harris,et al.  Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster , 1976, The Journal of physiology.

[95]  E. Wist,et al.  The spatial frequency effect on perceived velocity , 1976, Vision Research.

[96]  T. Poggio,et al.  The Volterra Representation and the Wiener Expansion: Validity and Pitfalls , 1977 .