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Modelling the Cellular Mechanisms of Fly Optic Flow Processing

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The Computing Dendrite

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 11))

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Abstract

Understanding the computational power of individual neurons is one of the major tasks in neuroscience. Complex calculations in dendrites and axons were identified in recent years in a great number of different systems. The small set of around 60 lobula plate tangential cells (LPTCs) in the fly visual system is a prime example where such computations and their underlying mechanisms are well understood. In this chapter we review recent findings resulting from detailed modelling studies based on experimental data from LPTCs. These studies have shown that the network connectivity is sufficient to explain the morphology of LPTCs to a large extent. Furthermore, an extensive network ubiquitously but highly selectively connects LPTC dendrites and axons with each other and is responsible for sophisticated optic flow calculations. The electrotonic features of LPTCs are affected by this network. We describe how a selective dendritic network between Horizontal System (HS) and Centrifugal Horizontal (CH) cells implements a specialised spatial filter operating on the moving images encoded in the dendrites. We also show how an axonal network renders the axon terminals of Vertical System (VS) cells in the fly selective to rotational optic flow. In summary, fly LPTCs are a prime example to show that the embedding and wiring within the network is crucial to understand morphology and computation.

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References

  • Bialek W, Rieke F, Ruyter D, van Steveninck RR, Warland DK (1991) Reading a neural code. Science 252:1854–1857

    Article  PubMed  CAS  Google Scholar 

  • Bock DD, Lee W-CA, Kerlin AM et al (2011) Network anatomy and in vivo physiology of visual cortical neurons. Nature 471:177–182

    Article  PubMed  CAS  Google Scholar 

  • Borst A (2012) Fly motion vision: from optic flow to visual course control. e-Neuroforum 3:59–66

    Article  Google Scholar 

  • Borst A, Egelhaaf M (1992) In vivo imaging of calcium accumulation in fly interneurons as elicited by visual motion stimulation. Proc Natl Acad Sci USA 89:4139–4143

    Article  PubMed  CAS  Google Scholar 

  • Borst A, Haag J (2002) Neural networks in the cockpit of the fly. J Comp Physiol A 188:419–437

    Article  CAS  Google Scholar 

  • Borst A, Haag J (2001) Effects of mean firing on neural information rate. J Comput Neurosci 10:213–221

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Borst A, Haag J, Reiff DF (2010) Fly motion vision. Annu Rev Neurosci 33:49–70

    Article  PubMed  CAS  Google Scholar 

  • Borst A, Single S (2000) Local current spread in electrically compact neurons of the fly. Neurosci Lett 285:123–126

    Article  PubMed  CAS  Google Scholar 

  • Borst A, Weber F (2011) Neural action fields for optic flow based navigation: a simulation study of the fly lobula plate network. PLoS ONE 6:e16303

    Article  PubMed  CAS  Google Scholar 

  • Branco T, Clark BA, Häusser M (2010) Dendritic discrimination of temporal input sequences in cortical neurons. Science 329:1671–1675

    Article  PubMed  CAS  Google Scholar 

  • Briggman KL, Helmstaedter M, Denk W (2011) Wiring specificity in the direction-selectivity circuit of the retina. Nature 471:183–188

    Article  PubMed  CAS  Google Scholar 

  • Cook JE, Becker DL (1995) Gap junctions in the vertebrate retina. Microsc Res Tech 31:408–419

    Article  PubMed  CAS  Google Scholar 

  • Cuntz H, Borst A, Segev I (2007a) Optimization principles of dendritic structure. Theor Biol Med Model 4:21

    Article  PubMed  Google Scholar 

  • Cuntz H, Forstner F, Borst A, Häusser M (2010) One rule to grow them all: a general theory of neuronal branching and its practical application. PLoS Comput Biol 6:e1000877

    Article  PubMed  Google Scholar 

  • Cuntz H, Forstner F, Haag J, Borst A (2008) The morphological identity of insect dendrites. PLoS Comput Biol 4:e1000251

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cuntz H, Haag J, Forstner F et al (2007b) Robust coding of flow-field parameters by axo-axonal gap junctions between fly visual interneurons. Proc Natl Acad Sci USA 104:10229–10233

    Article  PubMed  CAS  Google Scholar 

  • Cuntz H, Mathy A, Häusser M (2012) A scaling law derived from optimal dendritic wiring. Proc Natl Acad Sci USA 109:11014–11018

    Article  PubMed  CAS  Google Scholar 

  • Dürr V, Egelhaaf M (1999) In vivo calcium accumulation in presynaptic and postsynaptic dendrites of visual interneurons. J Neurophys 82:3327–3338

    Google Scholar 

  • Egelhaaf M (1985a) On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. I. Behavioural constraints imposed on the neuronal network. Biol Cybern 52:123–140

    Article  Google Scholar 

  • Egelhaaf M (1985b) On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. II. Figure-detection cells, a new class of visual interneurones. Biol Cybern 52:195–209

    Google Scholar 

  • Egelhaaf M (1985c) On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. III. Possible input circuitries and behavioural significance of the FD-cells. Biol Cybern 52:267–280

    Article  Google Scholar 

  • Egelhaaf M, Borst A (1995) Calcium accumulation in visual interneurons of the fly: stimulus dependence and relationship to membrane potential. J Neurophys 73:2540–2552

    CAS  Google Scholar 

  • Egelhaaf M, Haag J, Borst A (1994) Processing of synaptic information depends on the structure of the dendritic tree. Neuroreport 6:205–208

    Article  PubMed  CAS  Google Scholar 

  • Elyada YM, Haag J, Borst A (2009) Different receptive fields in axons and dendrites underlie robust coding in motion-sensitive neurons. Nat Neurosci 12:327–332

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Farrow K, Haag J, Borst A (2006) Nonlinear, binocular interactions underlying flow field selectivity of a motion-sensitive neuron. Nat Neurosci 9:1312–1320

    Article  PubMed  CAS  Google Scholar 

  • Gabbiani F, Krapp HG, Koch C, Laurent G (2002) Multiplicative computation in a visual neuron sensitive to looming. Nature 420:320–324

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Geiger G, Nässel DR (1981) Visual orientation behaviour of flies after selective laser beam ablation of interneurones. Nature 293:398–399

    Article  PubMed  CAS  Google Scholar 

  • Gidon A, Segev I (2012) Principles governing the operation of synaptic inhibition in dendrites. Neuron 75:330–341

    Article  PubMed  CAS  Google Scholar 

  • Grueber WB, Yang C-H, Ye B, Jan Y-N (2005) The development of neuronal morphology in insects. Curr Biol 15:R730–R738

    Article  PubMed  CAS  Google Scholar 

  • Haag J, Borst A (1996) Amplification of high-frequency synaptic inputs by active dendritic membrane processes. Nature 379:639–641

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Haag J, Borst A (2005) Dye-coupling visualizes networks of large-field motion-sensitive neurons in the fly. J Comp Physiol A 191:445–454

    Article  Google Scholar 

  • Haag J, Borst A (2000) Spatial distribution and characteristics of voltage-gated calcium signals within visual interneurons. J Neurophys 83:1039–1051

    CAS  Google Scholar 

  • Haag J, Borst A (2008) Electrical coupling of lobula plate tangential cells to a heterolateral motion-sensitive neuron in the fly. J Neurosci 28:14435–14442

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Haag J, Wertz A, Borst A (2007) Integration of lobula plate output signals by DNOVS1, an identified premotor descending neuron. J Neurosci 27:1992–2000

    Article  PubMed  CAS  Google Scholar 

  • Haag J, Wertz A, Borst A (2010) Central gating of fly optomotor response. Proc Natl Acad Sci USA 107:20104–20109

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Hausen K (1982b) 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

    Article  Google Scholar 

  • Homberg U, Heinze S, Pfeiffer K et al (2011) Central neural coding of sky polarization in insects. Philos Trans R Soc Lond B Biol Sci 366:680–687

    Article  PubMed  Google Scholar 

  • Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160:106–154

    PubMed  CAS  Google Scholar 

  • Hughes ME, Bortnick R, Tsubouchi A et al (2007) Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54:417–427

    Article  PubMed  CAS  Google Scholar 

  • Jacobs GA, Miller JP, Aldworth Z (2008) Computational mechanisms of mechanosensory processing in the cricket. J Exp Biol 211:1819–1828

    Article  PubMed  Google Scholar 

  • Kleinfeld D, Bharioke A, Blinder P et al (2011) Large-scale automated histology in the pursuit of connectomes. J Neurosci 31:16125–16138

    Article  PubMed  CAS  Google Scholar 

  • Krapp HG, Hengstenberg B, Hengstenberg R (1998) Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. J Neurophys 79:1902–1917

    CAS  Google Scholar 

  • Krapp HG, Hengstenberg R (1996) Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384:463–466

    Article  PubMed  CAS  Google Scholar 

  • Lang S, Dercksen VJ, Sakmann B, Oberlaender M (2011) Simulation of signal flow in 3D reconstructions of an anatomically realistic neural network in rat vibrissal cortex. Neural Netw 24:998–1011

    Article  PubMed  Google Scholar 

  • Laughlin SB (1999) Visual motion: dendritic integration makes sense of the world. Curr Biol 9:R15–R17

    Article  PubMed  CAS  Google Scholar 

  • London M, Häusser M (2005) Dendritic computation. Annu Rev Neurosci 28:503–532

    Article  PubMed  CAS  Google Scholar 

  • Marder E, Bucher D (2001) Central pattern generators and the control of rhythmic movements. Curr Biol 11:R986–R996

    Article  PubMed  CAS  Google Scholar 

  • Markram H (2006) The blue brain project. Nat Rev Neurosci 7:153–160

    Article  PubMed  CAS  Google Scholar 

  • Meyer EP, Matute C, Streit P, Nässel DR (1986) Insect optic lobe neurons identifiable with monoclonal antibodies to GABA. Histochemistry 84:207–216

    Article  PubMed  CAS  Google Scholar 

  • Ohki K, Chung S, Ch’ng YH et al (2005) Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433:597–603

    Article  PubMed  CAS  Google Scholar 

  • Peron SP, Jones PW, Gabbiani F (2009) Precise subcellular input retinotopy and its computational consequences in an identified visual interneuron. Neuron 63:830–842

    Article  PubMed  CAS  Google Scholar 

  • Rall W (1959) Branching dendritic trees and motoneuron membrane resistivity. Exp Neurol 527:491–527

    Article  Google Scholar 

  • Rall W, Rinzel J (1973) Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. Biophys J 13:648–687

    Article  PubMed  CAS  Google Scholar 

  • Reichardt W, Poggio T, Hausen K (1983) Figure-ground discrimination by relative movement in the visual system of the fly. Biol Cybern 46:1–30

    Article  Google Scholar 

  • Ruyter D, van Steveninck RR, Bialek W (1988) Real-time performance of a movement-sensitive neuron in the blowfly visual system: coding and information transfer in short spike sequences. Proc R Soc Lond B 234:379–414

    Article  Google Scholar 

  • Seung HS, Lee DD, Reis BY, Tank DW (2000) Stability of the memory of eye position in a recurrent network of conductance-based model neurons. Neuron 26:259–271

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Torben-Nielsen B, Stiefel KM (2010) Wide-field motion integration in fly vs cells: insights from an inverse approach. PLoS Comput Biol 6:e1000932

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Watt AJ, Cuntz H, Mori M et al (2009) Traveling waves in developing cerebellar cortex mediated by asymmetrical Purkinje cell connectivity. Nat Neurosci 12:463–473

    Article  PubMed  CAS  Google Scholar 

  • Wertz A, Borst A, Haag J (2008) Nonlinear integration of binocular optic flow by DNOVS2, a descending neuron of the fly. J Neurosci 28:3131–3140

    Article  PubMed  CAS  Google Scholar 

  • Wertz A, Gaub B, Plett J et al (2009) Robust coding of ego-motion in descending neurons of the fly. J Neurosci 29:14993–15000

    Article  PubMed  CAS  Google Scholar 

  • Wertz A, Haag J, Borst A (2012) Integration of binocular optic flow in cervical neck motor neurons of the fly. J Comp Physiol A 198:655–668

    Article  Google Scholar 

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Acknowledgement

The work presented here was a collaborative effort together with Friedrich Förstner and Idan Segev.

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Correspondence to Hermann Cuntz .

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Cuntz, H., Haag, J., Borst, A. (2014). Modelling the Cellular Mechanisms of Fly Optic Flow Processing. In: Cuntz, H., Remme, M., Torben-Nielsen, B. (eds) The Computing Dendrite. Springer Series in Computational Neuroscience, vol 11. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8094-5_16

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