Nonlinear, binocular interactions underlying flow field selectivity of a motion-sensitive neuron

Neurons in many species have large receptive fields that are selective for specific optic flow fields. Here, we studied the neural mechanisms underlying flow field selectivity in lobula plate tangential cells (LPTCs) of the blowfly. Among these cells, the H2 cell responds preferentially to visual stimuli approximating rotational optic flow. Through double recordings from H2 and many other LPTCs, we characterized a bidirectional commissural pathway that allows visual information to be shared between the hemispheres. This pathway is mediated by axo-axonal electrical coupling of H2 and the horizontal system equatorial (HSE) cell located in the opposite hemisphere. Using single-cell ablations, we found that this pathway is sufficient to allow H2 to amplify and attenuate dendritic input during binocular visual stimuli. This is accomplished through a modulation of H2's membrane potential by input from the contralateral HSE cell, which scales the firing rate of H2 during visual stimulation but is not sufficient to induce action potentials.

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

[2]  G. Schlotterer.  Response of the locust descending movement detector neuron to rapidly approaching and withdrawing visual stimuli , 1977 .

[3]  J. Miller,et al.  Rapid killing of single neurons by irradiation of intracellularly injected dye. , 1979, Science.

[4]  Hendrik Eckert,et al.  The centrifugal horizontal cells in the lobula plate of the blowfly, Phaenicia sericata , 1983 .

[5]  K. Hausen.  The Lobula-Complex of the Fly: Structure, Function and Significance in Visual Behaviour , 1984 .

[6]  R. Shapley,et al.  Photoreception and Vision in Invertebrates , 1984, NATO ASI Series.

[7]  J. Simpson,et al.  The accessory optic system of rabbit. I. Basic visual response properties. , 1988, Journal of neurophysiology.

[8]  J. Simpson,et al.  The accessory optic system of rabbit. II. Spatial organization of direction selectivity. , 1988, Journal of neurophysiology.

[9]  K. Tanaka,et al.  Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[10]  B J Frost,et al.  Binocular neurons in the nucleus of the basal optic root (nBOR) of the pigeon are selective for either translational or rotational visual flow , 1990, Visual Neuroscience.

[11]  A. Borst,et al.  Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques. , 1993, Journal of neurophysiology.

[12]  B. Frost,et al.  Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. I. Functional organization of neurons discriminating between translational and rotational visual flow. , 1993, Journal of neurophysiology.

[13]  M Egelhaaf,et al.  Neural circuit tuning fly visual neurons to motion of small objects. II. Input organization of inhibitory circuit elements revealed by electrophysiological and optical recording techniques. , 1993, Journal of neurophysiology.

[14]  G. Orban,et al.  Responses of macaque STS neurons to optic flow components: a comparison of areas MT and MST. , 1994, Journal of neurophysiology.

[15]  R. Hengstenberg,et al.  Estimation of self-motion by optic flow processing in single visual interneurons , 1996, Nature.

[16]  Alexander Borst,et al.  Synapse distribution on VCH, an inhibitory, motion‐sensitive interneuron in the fly visual system , 1997, The Journal of comparative neurology.

[17]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[18]  A. Borst,et al.  Dendritic integration and its role in computing image velocity. , 1998, Science.

[19]  Hateren,et al.  Blowfly flight and optic flow. II. Head movements during flight , 1999, The Journal of experimental biology.

[20]  G. Laurent,et al.  Computation of Object Approach by a Wide-Field, Motion-Sensitive Neuron , 1999, The Journal of Neuroscience.

[21]  Hateren,et al.  Blowfly flight and optic flow. I. Thorax kinematics and flight dynamics , 1999, The Journal of experimental biology.

[22]  Nicholas T. Carnevale,et al.  Expanding NEURON's Repertoire of Mechanisms with NMODL , 2000, Neural Computation.

[23]  M. Egelhaaf,et al.  Synaptic interactions increase optic flow specificity , 2000, The European journal of neuroscience.

[24]  R. Hengstenberg,et al.  Binocular contributions to optic flow processing in the fly visual system. , 2001, Journal of neurophysiology.

[25]  A Borst,et al.  Recurrent Network Interactions Underlying Flow-Field Selectivity of Visual Interneurons , 2001, The Journal of Neuroscience.

[26]  A. Borst,et al.  Dendro-Dendritic Interactions between Motion-Sensitive Large-Field Neurons in the Fly , 2002, The Journal of Neuroscience.

[27]  M. Srinivasan,et al.  Insect behaviour: Motion camouflage in dragonflies , 2003, Nature.

[28]  A. Borst,et al.  Orientation tuning of motion-sensitive neurons shaped by vertical-horizontal network interactions , 2003, Journal of Comparative Physiology A.

[29]  A. Borst,et al.  Input Organization of Multifunctional Motion-Sensitive Neurons in the Blowfly , 2003, The Journal of Neuroscience.

[30]  Alexander Borst,et al.  Neural image processing by dendritic networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[31]  A. Borst,et al.  The Intrinsic Electrophysiological Characteristics of Fly Lobula Plate Tangential Cells: II. Active Membrane Properties , 2004, Journal of Computational Neuroscience.

[32]  E. Meyer,et al.  Insect optic lobe neurons identifiable with monoclonal antibodies to GABA , 2004, Histochemistry.

[33]  Martina Medkovatt,et al.  Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio , 2004 .

[34]  A. Borst,et al.  Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons , 2004, Nature Neuroscience.

[35]  K. Hausen,et al.  The synaptic organization of visual interneurons in the lobula complex of flies , 1980, Cell and Tissue Research.

[36]  M. Srinivasan,et al.  Visual motor computations in insects. , 2004, Annual review of neuroscience.

[37]  Alexander Borst,et al.  The intrinsic electrophysiological characteristics of fly lobula plate tangential cells: I. Passive membrane properties , 1996, Journal of Computational Neuroscience.

[38]  A. Borst,et al.  Spatio-temporal integration of motion , 1988, The Science of Nature.

[39]  Alexander Borst,et al.  The Intrinsic Electrophysiological Characteristics of Fly Lobula Plate Tangential Cells: III. Visual Response Properties , 1999, Journal of Computational Neuroscience.

[40]  N. Strausfeld,et al.  The organization of giant horizontal-motion-sensitive neurons and their synaptic relationships in the lateral deutocerebrum of Calliphora erythrocephala and Musca domestica , 1985, Cell and Tissue Research.

[41]  K. Hausen.  Motion sensitive interneurons in the optomotor system of the fly , 1982, Biological Cybernetics.

[42]  A. Borst,et al.  Sharing Receptive Fields with Your Neighbors: Tuning the Vertical System Cells to Wide Field Motion , 2005, The Journal of Neuroscience.

[43]  K. Farrow.  Lateral Interactions and Receptive Field Structure of Lobula Plate Tangential Cells in the Blowfly , 2005 .

[44]  J. V. van Hateren,et al.  Function and Coding in the Blowfly H1 Neuron during Naturalistic Optic Flow , 2005, The Journal of Neuroscience.

[45]  Alexander Borst,et al.  Dye-coupling visualizes networks of large-field motion-sensitive neurons in the fly , 2005, Journal of Comparative Physiology A.

[46]  J. P. Lindemann,et al.  Function of a Fly Motion-Sensitive Neuron Matches Eye Movements during Free Flight , 2005, PLoS biology.

[47]  P. R. Green,et al.  Optic flow-field variables trigger landing in hawk but not in pigeons , 1990, Naturwissenschaften.

[48]  J. V. van Hateren,et al.  Encoding of naturalistic optic flow by a population of blowfly motion-sensitive neurons. , 2006, Journal of neurophysiology.

[49]  J. Golowasch,et al.  Signal transmission between gap-junctionally coupled passive cables is most effective at an optimal diameter. , 2006, Journal of neurophysiology.