Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

In locusts, two lobula giant movement detector neurons (LGMDs) act as looming object detectors. Their reproducible responses to looming and their ethological significance makes them models for single neuron computation. But there is no comprehensive picture of the neurons that connect directly to each LGMD. We used high-through-put serial block-face scanning-electron-microscopy to reconstruct the network of input-synapses onto the LGMDs over spatial scales ranging from single synapses and small circuits, up to dendritic branches and total excitatory input. Reconstructions reveal that many trans-medullary-afferents (TmAs) connect the eye with each LGMD, one TmA per facet per LGMD. But when a TmA synapses with an LGMD it also connects laterally with another TmA. These inter-TmA synapses are always reciprocal. Total excitatory input to the LGMD 1 and 2 comes from 131,000 and 186,000 synapses reaching densities of 3.1 and 2.6 synapses per μm 2 respectively. We explored the computational consequences of reciprocal synapses between each TmA and 6 others from neighbouring columns. Since any lateral interactions between LGMD inputs have always been inhibitory we may assume these reciprocal lateral connections are most likely inhibitory. Such reciprocal inhibitory synapses increased the LGMD's selectivity for looming over passing objects, particularly at the beginning of object approach. © The Author(s) 2016.

Registro:

Documento: Artículo
Título:Two identified looming detectors in the locust: Ubiquitous lateral connections among their inputs contribute to selective responses to looming objects
Autor:Rind, F.C.; Wernitznig, S.; Pölt, P.; Zankel, A.; Gütl, D.; Sztarker, J.; Leitinger, G.
Filiación:Institute of Neuroscience, Centre for Behaviour and Evolution, Newcastle University, Newcastle upon Tyne, NE1 7RU, United Kingdom
Institute of Cell Biology, Histology and Embryology/Research Unit Electron Microscopic Techniques, Graz, 8010, Austria
Institute for Electron Microscopy and Nanoanalysis/NAWI Graz, Graz University of Technology, Graz, 8010, Austria
Centre for Electron Microscopy, Graz, 8010, Austria
Departamento de Fisiologia, Biologia Molecular y Celular/FCEN, Universidad de Buenos Aires/IFIBYNE-CONICET, Buenos Aires, 1428, Argentina
BioTechMed-Graz, Graz, 8010, Austria
Año:2016
Volumen:6
DOI: http://dx.doi.org/10.1038/srep35525
Título revista:Scientific Reports
Título revista abreviado:Sci. Rep.
ISSN:20452322
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_20452322_v6_n_p_Rind

Referencias:

  • Barlow, H.B., Summation and inhibition in the frog?s retina (1953) J. Physiol., 119, pp. 69-88
  • Lettvin, J.Y., Maturana, H.R., McCulloch, W.S., Pitts, W.H., What the Frog?s eye tells the frog?s brain (1959) Proceedings of the Institute of Radio Engineers, 47, pp. 1940-1951
  • Takemura, S.-Y., A visual motion detection circuit suggested by Drosophila connectomics (2013) Nature, 500, pp. 175-181
  • Hatsopoulos, N., Gabbiani, F., Laurent, G., Elementary computation of object approach by a wide-field visual neuron (1995) Science, p. 1000
  • Rind, F.C., Simmons, P.J., Orthopteran DCMD neuron: A reevaluation of responses to moving objects. I. Selective responses to approaching objects (1992) J. Neurophysiol., 68, pp. 1654-1666
  • Simmons, P.J., Rind, F.C., Responses to object approach by a wide field visual neurone, the LGMD2 of the locust: Characterization and image cues (1997) J. Comp. Physiol. A., 180, pp. 203-214
  • Simmons, P.J., Sztarker, J., Rind, F.C., Looming detection by identified visual interneurons during larval development of the locust Locusta migratoria (2013) J. Exp. Biol., 216, pp. 2266-2275
  • Sztarker, J., Rind, F.C., A look into the cockpit of the developing locust: Looming detectors and predator avoidance (2014) Dev. Neurobiol., 74, pp. 1078-1095
  • Fotowat, H., Harrison, R.R., Gabbiani, F., Multiplexing of motor information in the discharge of a collision detecting neuron during escape behaviors (2011) Neuron, 69, pp. 147-158
  • Silva, A.C., McMillan, G.A., Santos, C.P., Gray, J.R., Background complexity affects response of a looming-sensitive neuron to object motion (2015) J. Neurophysiol., 113, pp. 218-231
  • Fotowat, H., Gabbiani, F., Collision detection as a model for sensory-motor integration (2011) Annu. Rev. Neurosci., 34, pp. 1-19
  • Santer, R.D., Yamawaki, Y., Rind, F.C., Simmons, P.J., Preparing for escape: An examination of the role of the DCMD neuron in locust escape jumps (2008) J. Comp. Physiol. A., 194, pp. 69-77
  • Santer, R.D., Rind, F.C., Simmons, P.J., Predator versus prey: Locust looming-detector neuron and behavioural responses to stimuli representing attacking bird predators (2012) PLoS One, 7, p. e50146
  • London, M., Häusser, M., Dendritic computation (2005) Annu. Rev. Neurosci., 28, pp. 503-532
  • Peron, S.P., Biophysical mechanisms of computation in a looming sensitive neuron (2014) The Computing Dendrite, pp. 277-293. , eds. Cuntz, H., Michiel W. H. Remme, M. W. H. Benjamin Torben-Nielsen, B.) Springer
  • Peron, S.P., Jones, P.W., Gabbiani, F., Precise subcellular input retinotopy and its computational consequences in an identified visual interneuron (2009) Neuron, 63, pp. 830-842
  • Jones, P.W., Gabbiani, F., Logarithmic compression of sensory signals within the dendritic tree of a collision-sensitive neuron (2012) J. Neurosci., 32, pp. 4923-4934
  • Rind, F.C., Simmons, P.J., Local circuit for the computation of object approach by an identified visual neuron in the locust (1998) J. Comp. Neurol., 395, pp. 405-415
  • Dick, P.C., Gray, J.R., Spatiotemporal stimulus properties modulate responses to trajectory changes in a locust looming-sensitive pathway (2014) J. Neurophysiol., 111, pp. 1736-1745
  • Jones, P.W., Gabbiani, F., Synchronized neural input shapes stimulus selectivity in a collision-detecting neuron (2010) Curr. Biol., 20, pp. 2052-2057
  • Peron, S.P., Gabbiani, F., Role of spike-frequency adaptation in shaping neuronal response to dynamic stimuli (2009) Biol. Cybern., 100, pp. 505-520
  • O'Shea, M., Rowell, C.H., Protection from habituation by lateral inhibition (1975) Nature
  • Pinter, R.B., Inhibition and excitation in the locust DCMD receptive field: Spatial frequency, temporal and spatial characteristics (1979) J. Exp. Biol., 80, pp. 191-216
  • Zhu, Y., Gabbiani, F., Fine and distributed subcellular retinotopy of excitatory inputs to the dendritic tree of a collision-detecting neuron (2016) J. Neurophysiol., 115, pp. 3101-3112
  • Rind, F.C., Leitinger, G., Immunocytochemical evidence that collision sensing neurons in the locust visual system contain acetylcholine (2000) J. Comp. Neurol., 423, pp. 389-401
  • Rind, F.C., Bramwell, D.I., Neural network based on the input organization of an identified neuron signaling impending collision (1996) J. Neurophysiol., 75, pp. 967-985
  • James, A.C., Osorio, D., Characterisation of columnar neurons and visual signal processing in the medulla of the locust optic lobe by system identification techniques (1996) J. Comp. Physiol. A., 178, pp. 183-199
  • Peron, S.P., Krapp, H.G., Gabbiani, F., Influence of electrotonic structure and synaptic mapping on the receptive field properties of a collision-detecting neuron (2007) J Neurophysiol, 97, pp. 159-177
  • Krapp, H.G., Gabbiani, F., Spatial distribution of inputs and local receptive field properties of a wide-field looming sensitive neuron (2005) J. Neurophysiol., 93, pp. 2240-2253
  • Denk, W., Horstmann, H., Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure (2004) Plos Biol, 2, pp. 1900-1909
  • Wernitznig, S., Synaptic connections of first-stage visual neurons in the locust Schistocerca gregaria extend evolution of tetrad synapses back 200 million years (2015) J. Comp. Neurol., 523, pp. 298-312
  • Rind, F.C., Non-directional movement sensitive neurones of the locust optic lobe (1987) J. Comp. Physiol., A161, pp. 477-494
  • Simmons, P.J., Postsynaptic potentials of limited duration in visual neurones of a locust (1985) J. Exp. Biol., 117, pp. 193-217
  • Gabbiani, F., Krapp, H.G., Koch, C., Laurent, G., Multiplicative computation in a visual neuron sensitive to looming (2002) Nature, 420, pp. 320-324
  • Peron, S., Gabbiani, F., Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron (2009) Nat. Neurosci., 12, pp. 318-326
  • Harris, J.J., Jolivet, R., Attwell, D., Synaptic energy use and supply (2012) Neuron, 75, pp. 762-777
  • Mishchenko, Y., Ultrastructural analysis of hippocampal neuropil from the connectomics perspective (2010) Neuron, 67, pp. 1009-1020
  • Meinertzhagen, I.A., Hu, X., Evidence for site selection during synaptogenesis: The surface distribution of synaptic sites in photoreceptor terminals of the flies Musca and Drosophila (1996) Cell Mol. Neurobiol., 16, pp. 677-698
  • Napper, R.M.A., Harvey, R.J., Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat (1988) J. Comp. Neurol., 274, pp. 168-177
  • Watson, A.H.D., Schürmann, F.-W., Synaptic structure, distribution, and circuitry in the central nervous system of the locust and related insects (2002) Micros. Res. Tech., 56, pp. 210-226
  • Branco, T., Clark, B.A., Häusser, M., Dendritic discrimination of temporal input sequences in cortical neurons (2010) Science, 329, pp. 1671-1675
  • O'Shea, M., Rowell, C.H., Protection from habituation by lateral inhibition (1975) Nature, 254, pp. 53-55
  • Shinomiya, K., Candidate neural substrates for off-edge motion detection in Drosophila (2014) Curr. Biol., 24, pp. 1062-1070
  • Collin, C., Two types of muscarinic acetylcholine receptors in Drosophila and other arthropods (2013) Cell. Mol. Life Sci., 70, pp. 3231-3242
  • Le Corronc, H., Lapied, B., Hue, B., M 2-like presynaptic receptors modulate acetylcholine release in the cockroach (Periplaneta americana) central nervous system (1991) J. Insect Physiol., 37, pp. 647-652
  • Hue, B., Lapied, B., Malecot, C.O., Short communication: Do presynaptic muscarinic receptors regulate acetylcholine release in the central nervous system of the cockroach periplaneta Americana? (1989) J. Exp. Biol., 142, pp. 447-451
  • Judge, S., Leitch, B., Modulation of transmitter release from the locust forewing stretch receptor neuron by GABAergic interneurons activated via muscarinic receptors (1999) J. Neurobiol., 40, pp. 420-431
  • Gibson, J.J., Visually controlled locomotion and visual orientation in animals (1958) Br. J. Psychol., 49, pp. 182-194
  • Simmons, P.J., Rind, F.C., Orthopteran DCMD neuron: A reevaluation of responses to moving objects. II. Critical cues for detecting approaching objects (1992) J. Neurophysiol., 68, pp. 1667-1682
  • Santer, R.D., Rind, F.C., Stafford, R., Simmons, P.J., Role of an identified looming-sensitive neuron in triggering a flying locust?s escape (2006) J. Neurophysiol., 95, pp. 3391-3400
  • Gabbiani, F., Krapp, H.G., Laurent, G., Computation of object approach by a wide-field, motion-sensitive neuron (1999) J. Neurosci., 19, pp. 1122-1141
  • De Vries, S.E.J., Clandinin, T.R., Loom-sensitive neurons link computation to action in the Drosophila visual system (2012) Curr. Biol., 22, pp. 353-362
  • Sun, H., Frost, B.J., Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons (1998) Nat. Neurosci, 1, pp. 296-303
  • Nakagawa, H., Hongjian, K., Collision-sensitive neurons in the optic tectum of the bullfrog Rana catesbeiana (2010) J. Neurophysiol., 104, pp. 2487-2499
  • Preuss, T., Osei-Bonsu, P.E., Weiss, S.A., Wang, C., Faber, D.S., Neural representation of object approach in a decision-making motor circuit (2006) J. Neurosci., 26, pp. 3454-3464
  • Liu, Y.J., Wang, Q., Li, B., Neuronal responses to looming objects in the superior colliculus of the cat (2011) Brain. Behav. Evol., 77, pp. 193-205
  • Rind, F.C., Identification of directionally selective motion-detecting neurones in the locust lobula and their synaptic connections with an identified descending neurone (1990) J. Exp. Biol., 149, pp. 21-43
  • Fiala, J.C., Reconstruct: A free editor for serial section microscopy (2005) J Microsc-Oxford, 218, pp. 52-61
  • Deerinck, T.J., Enhancing serial block-face scanning electron microscopy to enable high resolution 3-d nanohistology of cells and tissues (2010) Microsc. Microanal., 16, p. 1138
  • Leitinger, G., Structural organization of the presynaptic density at identified synapses in the locust central nervous system (2012) J. Comp. Neurol., 520, pp. 384-400
  • Wernitznig, S., Zankel, A., Pölt, P., Rind, C., Leitinger, G., Investigation of neurons in the visual system of the locust Locusta migratoria with Serial Block Face Scanning Electron Microscopy (SBEM) Front. Physiol
  • Rowell, C.H.F., The orthopteran descending movement detector (DMD) neurones: A characterisation and review (1971) Z. Vgl. Physiol., 73, pp. 167-194

Citas:

---------- APA ----------
Rind, F.C., Wernitznig, S., Pölt, P., Zankel, A., Gütl, D., Sztarker, J. & Leitinger, G. (2016) . Two identified looming detectors in the locust: Ubiquitous lateral connections among their inputs contribute to selective responses to looming objects. Scientific Reports, 6.
http://dx.doi.org/10.1038/srep35525
---------- CHICAGO ----------
Rind, F.C., Wernitznig, S., Pölt, P., Zankel, A., Gütl, D., Sztarker, J., et al. "Two identified looming detectors in the locust: Ubiquitous lateral connections among their inputs contribute to selective responses to looming objects" . Scientific Reports 6 (2016).
http://dx.doi.org/10.1038/srep35525
---------- MLA ----------
Rind, F.C., Wernitznig, S., Pölt, P., Zankel, A., Gütl, D., Sztarker, J., et al. "Two identified looming detectors in the locust: Ubiquitous lateral connections among their inputs contribute to selective responses to looming objects" . Scientific Reports, vol. 6, 2016.
http://dx.doi.org/10.1038/srep35525
---------- VANCOUVER ----------
Rind, F.C., Wernitznig, S., Pölt, P., Zankel, A., Gütl, D., Sztarker, J., et al. Two identified looming detectors in the locust: Ubiquitous lateral connections among their inputs contribute to selective responses to looming objects. Sci. Rep. 2016;6.
http://dx.doi.org/10.1038/srep35525