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

Nature Neuroscience volume 9, pages 1312–1320 (2006)Cite this article

Abstract

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.

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Figure 1: Network connections.
Figure 2: Flow field selectivity of H2.
Figure 3: Double intracellular recording of H2 and HSE cells in opposite hemispheres.
Figure 4: Connectivity between H2 and the different HS and CH cells located in the opposite lobula plate.
Figure 5: H2 EPSP comparison.
Figure 6: Double ablations of ipsilateral CH cells.
Figure 7: Block of HS and CH cells in the opposite hemisphere.
Figure 8: Simulations of experiments shown in Figure 7.

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References

  1. Borst, A. & Bahde, S. Spatio-temporal integration of motion: a simple strategy for safe landing in flies. Naturwissenschaften 75, 265–267 (1988).

    Article  Google Scholar 

  2. Davies, M.N.O. & Green, P.R. Optic flow-field variables trigger landing in hawk but not in pigeons. Naturwissenschaften 77, 142–144 (1990).

    Article  CAS  Google Scholar 

  3. Mizutani, A., Chahl, J.S. & Srinivasan, M.V. Insect behaviour: motion camouflage in dragonflies. Nature 423, 604 (2003).

    Article  CAS  Google Scholar 

  4. Srinivasan, M.V. & Zhang, S. Visual motor computations in insects. Annu. Rev. Neurosci. 27, 679–696 (2004).

    Article  CAS  Google Scholar 

  5. Lagae, L., Maes, H., Raiguel, S., Xiao, D.K. & Orban, G.A. Responses of macaque STS neurons to optic flow components: a comparison of areas MT and MST. J. Neurophysiol. 71, 1597–1626 (1994).

    Article  CAS  Google Scholar 

  6. Tanaka, K. & Saito, H. 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. J. Neurophysiol. 62, 626–641 (1989).

    Article  CAS  Google Scholar 

  7. Soodak, R.E. & Simpson, J.I. The accessory optic system of rabbit. I. Basic visual response properties. J. Neurophysiol. 60, 2037–2054 (1988).

    Article  CAS  Google Scholar 

  8. Simpson, J.I., Leonard, C.S. & Soodak, R.E. The accessory optic system of rabbit. II. Spatial organization of direction selectivity. J. Neurophysiol. 60, 2055–2072 (1988).

    Article  CAS  Google Scholar 

  9. Wylie, D.R. & Frost, B.J. Binocular neurons in the nucleus of the basal optic root (nBOR) of the pigeon are selective for either translational or rotational visual flow. Vis. Neurosci. 5, 489–495 (1990).

    Article  CAS  Google Scholar 

  10. Wylie, D.R., Kripalani, T. & Frost, B.J. Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation. I. Functional organization of neurons discriminating between translational and rotational visual flow. J. Neurophysiol. 70, 2632–2646 (1993).

    Article  CAS  Google Scholar 

  11. Schlotterer, G.R. Response of the locust descending movement detector neuron to rapidly approaching and withdrawing visual stimuli. Can. J. Zool. 55, 1372–1376 (1977).

    Article  Google Scholar 

  12. Gabbiani, F., Krapp, H.G. & Laurent, G. Computation of object approach by wide-field, motion-sensitive neuron. J. Neurosci. 19, 1122–1141 (1999).

    Article  CAS  Google Scholar 

  13. Hausen, K. The lobula-complex of the fly: structure, function and significance in visual behaviour. in Photoreception and Vision in Invertebrates (ed. Ali, M.A.) 523–559 (Plenum Press, New York, 1984).

    Chapter  Google Scholar 

  14. Krapp, H.G. & Hengstenberg, R. Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384, 463–466 (1996).

    Article  CAS  Google Scholar 

  15. Krapp, H.G., Hengstenberg, R. & Egelhaaf, M. Binocular contributions to optic flow processing in the fly visual system. J. Neurophysiol. 85, 724–734 (2001).

    Article  CAS  Google Scholar 

  16. Haag, J. & Borst, A. Recurrent network interactions underlying flow-field selectivity of visual interneurons. J. Neurosci. 21, 5685–5692 (2001).

    Article  CAS  Google Scholar 

  17. Haag, J. & Borst, A. Orientation tuning of motion-sensitive neurons shaped by vertical-horizontal network interactions. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 189, 363–370 (2003).

    CAS  PubMed  Google Scholar 

  18. Kern, R., van Hateren, J.H., Michaelis, C., Lindemann, J.P. & Egelhaaf, M. Function of a fly motion-sensitive neuron matches eye movements during free flight. PLoS Biol. 3, e171 (2005).

    Article  Google Scholar 

  19. van Hateren, J.H., Kern, R., Schwerdtfeger, G. & Egelhaaf, M. Function and coding in the blowfly H1 neuron during naturalistic optic flow. J. Neurosci. 25, 4343–4352 (2005).

    Article  CAS  Google Scholar 

  20. Single, S. & Borst, A. Dendritic integration and its role in computing image velocity. Science 281, 1848–1850 (1998).

    Article  CAS  Google Scholar 

  21. Haag, J., Denk, W. & Borst, A. Fly motion vision is based on Reichardt detectors regardless of the signal-to-noise ratio. Proc. Natl. Acad. Sci. USA 101, 16333–16338 (2004).

    Article  CAS  Google Scholar 

  22. Warzecha, A.K., Egelhaaf, M. & Borst, A. Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques. J. Neurophysiol. 69, 329–339 (1993).

    Article  CAS  Google Scholar 

  23. Egelhaaf, M., Borst, A., Warzecha, A.K., Flecks, S. & Wildemann, A. 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. J. Neurophysiol. 69, 340–351 (1993).

    Article  CAS  Google Scholar 

  24. Horstmann, W., Egelhaaf, M. & Warzecha, A.K. Synaptic interaction increase optic flow specificity. Eur. J. Neurosci. 12, 2157–2165 (2000).

    Article  CAS  Google Scholar 

  25. Haag, J. & Borst, A. Dendro-dendritic interactions between motion-sensitive large-field neurons in the fly. J. Neurosci. 22, 3227–3233 (2002).

    Article  CAS  Google Scholar 

  26. Farrow, K., Haag, J. & Borst, A. Input organization of multifunctional motion-sensitive neurons in the blowfly. J. Neurosci. 23, 9805–9811 (2003).

    Article  CAS  Google Scholar 

  27. Haag, J. & Borst, A. Neural mechanism underlying complex receptive field properties of motion-sensitive interneurons. Nat. Neurosci. 7, 628–634 (2004).

    Article  CAS  Google Scholar 

  28. Farrow, K. Lateral interactions and receptive field structure of lobula plate tangential cells in the blowfly. Thesis, Ludwig-Maximilians-Universität, (2005).

  29. Hausen, K. Motion sensitive interneurons in the optomotor system of the fly. I. The horizontal cells: structure and signals. Biol. Cybern. 45, 143–156 (1982).

    Article  Google Scholar 

  30. Hausen, K. Motion sensitive interneurons in the optomotor system of the fly. II. The horizontal cells: receptive field organization and response characteristics. Biol. Cybern. 46, 67–79 (1982).

    Article  Google Scholar 

  31. Eckert, H. & Dvorak, D.R. The centrifugal horizontal cells in the lobula plate of the blowfly Phaenicia sericata. J. Insect Physiol. 29, 547–560 (1983).

    Article  Google Scholar 

  32. Hausen, K. Monocular and binocular computation of motion in the lobula plate of the fly. Verh. Dtsch. Zool. Ges. 74, 49–70 (1981).

    Google Scholar 

  33. Haag, J., Vermeulen, A. & Borst, A. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells: III. Visual response properties. J. Comput. Neurosci. 7, 213–234 (1999).

    Article  CAS  Google Scholar 

  34. Meyer, E.P., Matute, C., Streit, P. & Nassel, D.R. Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84, 207–216 (1986).

    Article  CAS  Google Scholar 

  35. Gauck, V., Egelhaaf, M. & Borst, A. Synapse distribution on VCH, an inhibitory, motion-sensitive interneuron in the fly visual system. J. Comp. Neurol. 381, 489–499 (1997).

    Article  CAS  Google Scholar 

  36. Haag, J. & Borst, A. Dye-coupling visualizes networks of large-field motion-sensitive neurons in the fly. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191, 445–454 (2005).

    Article  Google Scholar 

  37. Borst, A. & Haag, J. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells: I. Passive membrane properties. J. Comput. Neurosci. 3, 313–336 (1996).

    Article  CAS  Google Scholar 

  38. Haag, J., Theunissen, F. & Borst, A. The intrinsic electrophysiological characteristics of fly lobula plate tangential cells: II. Active membrane properties. J. Comput. Neurosci. 4, 349–369 (1997).

    Article  CAS  Google Scholar 

  39. Strausfeld, N.J. & Bassemir, U.K. The organization of giant horizontal-motion-sensitive neurons and their synaptic relationships in the lateral deutocerebrum of Calliphora erythrocephala and Musca domestica. Cell Tissue Res. 242, 531–550 (1985).

    Google Scholar 

  40. Cuntz, H., Haag, J. & Borst, A. Neural image processing by dendritic networks. Proc. Natl. Acad. Sci. USA 100, 11082–11085 (2003).

    Article  CAS  Google Scholar 

  41. Hausen, K., Wolburg-Buchholz, K. & Ribi, W.A. The synaptic organization of visual interneurons in the lobula complex of flies. Cell Tissue Res. 208, 371–387 (1980).

    Article  CAS  Google Scholar 

  42. Nadim, F. & Golowasch, J. Signal transmission between gap-junctionally coupled passive cables is most effective at an optimal diameter. J. Neurophysiol. 95, 3831–3843 (2006).

    Article  Google Scholar 

  43. Land, M.F. Head movement of flies during visually guided flight. Nature 243, 299–300 (1973).

    Article  Google Scholar 

  44. Hateren, J.H. & Schilstra, C. Blowfly flight and optic flow. II. Head movements during flight. J. Exp. Biol. 202, 1491–1500 (1999).

    PubMed  Google Scholar 

  45. Schilstra, C. & Hateren, J.H. Blowfly flight and optic flow. I. Thorax kinematics and flight dynamics. J. Exp. Biol. 202, 1481–1490 (1999).

    PubMed  Google Scholar 

  46. Karmeier, K., van Hateren, J.H., Kern, R. & Egelhaaf, M. Encoding of naturalistic optic flow by a population of blowfly motion sensitive neurons. J. Neurophysiol. 96, 1602–1614 (2006).

    Article  CAS  Google Scholar 

  47. Farrow, K., Borst, A. & Haag, J. Sharing receptive fields with your neighbors: tuning the vertical system cells to wide field motion. J. Neurosci. 25, 3985–3993 (2005).

    Article  CAS  Google Scholar 

  48. Miller, J.P. & Selverston, A. Rapid killing of single neurons by irradiation of intracellularly injected dye. Science 206, 702–704 (1979).

    Article  CAS  Google Scholar 

  49. Hines, M.L. & Carnevale, N.T. The NEURON simulation environment. Neural Comput. 9, 1179–1209 (1997).

    Article  CAS  Google Scholar 

  50. Hines, M.L. & Carnevale, N.T. Expanding NEURON's repertoire of mechanisms with NMODL. Neural Comput. 12, 995–1007 (2000).

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank R.H. Masland for carefully reading an earlier version of this manuscript.

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Author notes

  1. Karl Farrow

    Present address: Massachusetts General Hospital, Harvard Medical School, 50 Blossom Street, Thier 429, Boston, Massachusetts, 02114, USA

  2. Karl Farrow and Juergen Haag: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Systems and Computational Neurobiology, Max-Planck-Institute of Neurobiology, Am Klopferspitz 18, Martinsried, 82152, Germany

    Karl Farrow, Juergen Haag & Alexander Borst

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Contributions

K.F. and J.H. performed the experiments and analyzed the data. K.F. carried out the computer simulations. K.F., J.H. and A.B. jointly planned the experiments, discussed the results and wrote the manuscript.

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Correspondence to Karl Farrow.

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Farrow, K., Haag, J. & Borst, A. Nonlinear, binocular interactions underlying flow field selectivity of a motion-sensitive neuron. Nat Neurosci 9, 1312–1320 (2006). https://doi.org/10.1038/nn1769

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