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Dye-coupling visualizes networks of large-field motion-sensitive neurons in the fly

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Abstract

In the fly, visually guided course control is accomplished by a set of 60 large-field motion-sensitive neurons in each brain hemisphere. These neurons have been shown to receive retinotopic motion information from local motion detectors on their dendrites. In addition, recent experiments revealed extensive coupling between the large-field neurons through electrical synapses. These two processes together give rise to their broad and elaborate receptive fields significantly surpassing the extent of their dendritic fields. Here, we demonstrate that the electrical connections between different large-field neurons can be visualized using Neurobiotin dye injection into a single one of them. When combined with a fluorescent dye which does not cross electrical synapses, the injected cell can be identified unambiguously. The Neurobiotin staining corroborates the electrical coupling postulated amongst the cells of the vertical system (VS-cells) and between cells of the horizontal system (HS-cells and CH-cells). In addition, connections between some cells are revealed that have so far not been considered as electrically coupled.

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Abbreviations

VS:

Vertical system

HS:

Horizontal system

CH:

Centrifugal horizontal

References

  • Basu AC, Kravitz EA (2003) Morphology and monoaminergic modulation of Crustacean Hyperglycemic Hormone-like immunoreactive neurons in the lobster nervous system J Neurocytol 32:253–263

    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

    Google Scholar 

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

    Google Scholar 

  • Chan WP, Prete F, Dickinson MH (1998) Visual input to the efferent control system of a fly’s “gyroscope”. Science 280:289–292

    Google Scholar 

  • Connors BW, Long MA (2004) Electrical synapses in the mammalian brain. Annu Rev Neurosci 27:393–418

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Gilbert C, Gronenberg W, Strausfeld NJ (1995) Oculomotor control in calliphorid flies: head movements during activation and inhibition of neck motor neurons corroborate neuroanatomical predictions. J Comp Neurol 361:285–297

    Google Scholar 

  • Gronenberg W, Strausfeld NJ (1990) Descending neurons supplying the neck and flight motor of diptera: physiological and anatomical characteristics. J Comp Neurol 302:973–991

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Haag J, Borst A (2003) Orientation tuning of motion-sensitive neurons shaped by vertical-horizontal network interactions. J Comp Physiol 189:363–370

    Google Scholar 

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

    Google Scholar 

  • Haag J, Egelhaaf M, Borst A (1992) Dendritic integration of motion information in visual interneurons of the blowfly. Neurosci Lett 140:173–176

    Google Scholar 

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

    Google Scholar 

  • Hausen K (1984) The lobula-complex of the fly: structure, function and significance in visual behaviour. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum Press, New York, pp 523–559

    Google Scholar 

  • Hengstenberg R, Hausen K, Hengstenberg B (1982) The number and structure of giant vertical cells (VS) in the lobula plate of the blowfly Calliphora erytrocephala. J Comp Physiol A 149:163–177

    Google Scholar 

  • Hornstein EP, Verweij J, Schnapf JL (2004) Electrical coupling between red and green cones in primate retina. Nat Neurosci 7:745–750

    Google Scholar 

  • Horstmann W, Egelhaaf M, Warzecha AK (2000) Synaptic interactions increase optic flow specificity. Eur J Neurosci 12:2157–2165

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Krapp HG, Hengstenberg R, Egelhaaf M (2001) Binocular contributions to optic flow processing in the fly visual system. J Neurophysiol 85(2):724–734

    Google Scholar 

  • Li W, DeVries S (2004) Separate blue and green cone networks in the mammalian retina. Nat Neurosci 7:751–756

    Google Scholar 

  • Mills SL, Massey SC (1995) Differential properties of two gap junctional pathways made by AII amacrine cells. Nature 377:734–737

    Google Scholar 

  • Mills SL, Massey SC (1998) The kinetics of tracer movement through homologous gap junctions in the rabbit retina. Vis Neurosci 15:765–777

    Google Scholar 

  • Mills SL, Massey SC (2000) A series of biotinylated tracers distinguishes three types of gap junction in retina. J Neurosci 20:8629–8636

    Google Scholar 

  • Penn AA, Wong ROL, Shatz CJ (1994) Neuronal coupling in the developing mammalian retina. J Neurosci 14:3805 3815

    Google Scholar 

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

    Google Scholar 

  • Stebbings LA, Todman MG, Phillips R, Greer CE, Tam J, Phelan P, Jacobs K, Bacon JP, Davies JA (2002) Gap junctions in Drosophila: developmental expression of the entire innexin gene family. Mech Dev 113:197–205

    Google Scholar 

  • Strausfeld NJ, Bassemir UK (1985a) Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg motor neuropil in Calliphora erythrocephala. Cell Tissue Res 240:617–640

    Google Scholar 

  • Strausfeld NJ, Bassemir UK (1985b) 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

    Google Scholar 

  • Szabo TM, Faber DS, Zoran MJ (2004) Transient electrical coupling delays the onset of chemical neurotransmission at developing synapses. J Neurosci 24:112–120

    Google Scholar 

  • Warzecha AK, 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 Neurophysiol 69:329–339

    Google Scholar 

  • Zahs KR, Newman EA (1997) Asymmetric gap junctional coupling between glial cells in the rat retina. GLIA 20(1):10–22

    Google Scholar 

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Acknowledgements

We are grateful to Renate Gleich and Dietmute Bueringer for excellent technical assistance. This work was supported by the Max-Planck Society.

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Correspondence to Juergen Haag.

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Haag, J., Borst, A. Dye-coupling visualizes networks of large-field motion-sensitive neurons in the fly. J Comp Physiol A 191, 445–454 (2005). https://doi.org/10.1007/s00359-005-0605-0

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