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Abstract:

Insect larvae clearly react to visual stimuli, but the ability of any visual neuron in a newly hatched insect to respond selectively to particular stimuli has not been directly tested. We characterised a pair of neurons in locust larvae that have been extensively studied in adults, where they are known to respond selectively to objects approaching on a collision course: the lobula giant motion detector (LGMD) and its postsynaptic partner, the descending contralateral motion detector (DCMD). Our physiological recordings of DCMD axon spikes reveal that at the time of hatching, the neurons already respond selectively to objects approaching the locust and they discriminate between stimulus approach speeds with differences in spike frequency. For a particular approaching stimulus, both the number and peak frequency of spikes increase with instar. In contrast, the number of spikes in responses to receding stimuli decreases with instar, so performance in discriminating approaching from receding stimuli improves as the locust goes through successive moults. In all instars, visual movement over one part of the visual field suppresses a response to movement over another part. Electron microscopy demonstrates that the anatomical substrate for the selective response to approaching stimuli is present in all larval instars: small neuronal processes carrying information from the eye make synapses both onto LGMD dendrites and with each other, providing pathways for lateral inhibition that shape selectivity for approaching objects. © 2013. Published by The Company of Biologists Ltd.

Registro:

Documento: Artículo
Título:Looming detection by identified visual interneurons during larval development of the locust Locusta migratoria
Autor:Simmons, P.J.; Sztarker, J.; Rind, F.C.
Filiación:Institute of Neuroscience, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom
Departamento de Fisiología, Biología Molecular y Celular, FCEN, Universidad de Buenos Aires, Pabellon 2 Ciudad Universitaria, Intendente Guiraldes 2160, Buenos Aires 1428, Argentina
Palabras clave:Development; Insect; Larva; Looming; Synapse; Vision; animal; article; development; electrophysiology; growth, development and aging; insect; interneuron; larva; Locusta migratoria; looming; movement perception; optic lobe; photostimulation; physiology; synapse; transmission electron microscopy; ultrastructure; vision; visual system; development; insect; larva; looming; synapse; vision; Animals; Electrophysiology; Interneurons; Larva; Locusta migratoria; Microscopy, Electron, Transmission; Motion Perception; Optic Lobe, Nonmammalian; Photic Stimulation; Visual Pathways; Acrididae; Arthropoda; Hexapoda; Locusta migratoria
Año:2013
Volumen:216
Número:12
Página de inicio:2266
Página de fin:2275
DOI: http://dx.doi.org/10.1242/jeb.083360
Título revista:Journal of Experimental Biology
Título revista abreviado:J. Exp. Biol.
ISSN:00220949
CODEN:JEBIA
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00220949_v216_n12_p2266_Simmons.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00220949_v216_n12_p2266_Simmons

Referencias:

  • Anderson, H., Postembryonic development of the visual system of the locust, Schistocerca gregaria. I. Patterns of growth and developmental interactions in the retina and optic lobe (1978) J. Embryol. Exp. Morphol., 45, pp. 55-83
  • Anderson, H., Bacon, J., Developmental determination of neuronal projection patterns from wind-sensitive hairs in the locust, Schistocerca gregaria (1979) Dev. Biol., 72, pp. 364-373
  • Bazazi, S., Buhl, J., Hale, J.J., Anstey, M.L., Sword, G.A., Simpson, S.J., Couzin, I.D., Collective motion and cannibalism in locust migratory bands (2008) Curr. Biol., 18, pp. 735-739
  • Bentley, D., Toroian-Raymond, A., Embryonic and postembryonic morphogenesis of a grasshopper interneuron (1981) J. Comp. Neurol., 201, pp. 507-518
  • Bernard, F., Récherches sur la morphogenèse des yeux composés d'arthropodes (1937) Bull. Biol. Fr. Belg., 23 (SUPPL.), pp. 1-162
  • Bloom, J.W., Atwood, H.L., Effects of altered sensory experience on the responsiveness of the locust descending contralateral movement detector neuron (1980) J. Comp. Physiol. A, 135, pp. 191-199
  • Boyan, G.S., Postembryonic development in the auditory system of the locust. Anatomical and physiological characterisation of interneurones ascending to the brain (1983) J. Comp. Physiol. A, 151, pp. 499-513
  • Bucher, D., Pflüger, H.J., Directional sensitivity of an identified windsensitive interneuron during the postembryonic development of the locust (2000) J. Insect Physiol., 46, pp. 1545-1556
  • Dangles, O., Pierre, D., Christides, J.P., Casas, J., Escape performance decreases during ontogeny in wild crickets (2007) J. Exp. Biol., 210, pp. 3165-3170
  • 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
  • Dewell, R.B., Gabbiani, F., Escape behavior: Linking neural computation to action (2012) Curr. Biol., 22, pp. R152-R153
  • Fotowat, H., Gabbiani, F., Relationship between the phases of sensory and motor activity during a looming-evoked multistage escape behavior (2007) J. Neurosci., 27, pp. 10047-10059
  • 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
  • Gray, J.R., Blincow, E., Robertson, R.M., A pair of motion-sensitive neurons in the locust encode approaches of a looming object (2010) J. Comp. Physiol. A, 196, pp. 927-938
  • Hatsopoulos, N., Gabbiani, F., Laurent, G., Elementary computation of object approach by wide-field visual neuron (1995) Science, 270, pp. 1000-1003
  • Horridge, G.A., The separation of visual axes in apposition compound eyes (1978) Philos. Trans. R. Soc. Lond. B, 285, pp. 1-59
  • Karmeier, K., Tabor, R., Egelhaaf, M., Krapp, H.G., Early visual experience and the receptive-field organization of optic flow processing interneurons in the fly motion pathway (2001) Vis. Neurosci., 18, pp. 1-8
  • Kirschfeld, K., The resolution of lens and compound eyes (1976) Neural Principles of Vision, pp. 356-370. , (ed. F. Zettler and R. Weiler) New York, NY: Springer
  • Kral, K., Poteser, M., Relationship between body size and spatial vision in the praying mantis - An ontogenetic study (2009) J. Orthoptera Res., 18, pp. 153-158
  • 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
  • Leitch, B., Laurent, G., Shepherd, D., Embryonic development of synapses on spiking local interneurones in locust (1992) J. Comp. Neurol., 324, pp. 213-236
  • Michel, K.J., Petersen, M., Development of the tympanal organ in larvae of the migratory locust (Locusta migratoria) (1982) Cell Tissue Res., 222, pp. 667-676
  • Newland, P.L., Watkins, B., Emptage, N.J., Nagayama, T., The structure, response properties and development of a hair plate on the mesothoracic leg of the locust (1995) J. Exp. Biol., 198, pp. 2397-2404
  • O'Shea, M., Rowell, C.H.F., Protection from habituation by lateral inhibition (1975) Nature, 254, pp. 53-55
  • O'Shea, M., Rowell, C.H.F., A spike-transmitting electrical synapse between visual interneurons in the locust movement detector system (1975) J. Comp. Physiol., 97, pp. 143-158
  • O'Shea, M., Rowell, C.H.F., The neuronal basis of a sensory analyser, the acridid movement detector system. II. response decrement, convergence, and the nature of the excitatory afferents to the fan-like dendrites of the LGMD (1976) J. Exp. Biol., 65, pp. 289-308
  • O'Shea, M., Williams, J.L.D., The anatomy and output connections of a locust visual interneurone: The lobula giant movement detector (LGMD) neurone (1974) J. Comp. Physiol., 91, pp. 257-266
  • Oliva, D., Medan, V., Tomsic, D., Escape behavior and neuronal responses to looming stimuli in the crab Chasmagnathus granulatus (Decapoda: Grapsidae) (2007) J. Exp. Biol., 210, pp. 865-880
  • Peron, S., Gabbiani, F., Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron (2009) Nat. Neurosci., 12, pp. 318-326
  • 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
  • Pflüger, H.J., Hurdelbrink, S., Czjzek, A., Burrows, M., Activity-dependent structural dynamics of insect sensory fibers (1994) J. Neurosci., 14, pp. 6946-6955
  • Pinter, R.B., Visual discrimination between small objects and large textured backgrounds (1977) Nature, 270, pp. 429-431
  • 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
  • Rafi, F., Burtt, E., Visual acuity in larval instars of Schistocerca gregaria and adults of two other orthopterans, Acridoidea (1974) Zool. Anz., 193, pp. 305-313
  • Rind, F.C., A chemical synapse between two motion detecting neurones in the locust brain (1984) J. Exp. Biol., 110, pp. 143-167
  • 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
  • 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., 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
  • 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
  • Rind, F.C., Santer, R.D., Wright, G.A., Arousal facilitates collision avoidance mediated by a looming sensitive visual neuron in a flying locust (2008) J. Neurophysiol., 100, pp. 670-680
  • Rogers, S.M., Krapp, H.G., Burrows, M., Matheson, T., Compensatory plasticity at an identified synapse tunes a visuomotor pathway (2007) J. Neurosci., 27, pp. 4621-4633
  • Rowell, C.H.F., The orthopteran descending movement detector (DMD) neurones: A characterisation and review (1971) J. Comp. Physiol., 73, pp. 167-194
  • Rowell, C.H.F., O'Shea, M., Williams, J.L., The neuronal basis of a sensory analyser, the acridid movement detector system. IV. The preference for small field stimuli (1977) J. Exp. Biol., 68, pp. 157-185
  • 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
  • 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, pp. e50146
  • Schlotterer, G., Response of the locust descending movement detector neuron to rapidly approaching and withdrawing visual stimuli (1977) Can. J. Zool., 55, pp. 1372-1376
  • Sehnal, F., Morphology of insect development (1985) Annu. Rev. Entomol., 30, pp. 89-109
  • 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
  • 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
  • Spaethe, J., Chittka, L., Interindividual variation of eye optics and single object resolution in bumblebees (2003) J. Exp. Biol., 206, pp. 3447-3453
  • Wilson, M., Garrard, P., McGinness, S., The unit structure of the locust compound eye (1978) Cell Tissue Res., 195, pp. 205-226
  • Zollikofer, C.P.E., Wehner, R., Fukushi, T., Optical scaling in conspecific Cataglyphis ants (1995) J. Exp. Biol., 198, pp. 1637-1646

Citas:

---------- APA ----------
Simmons, P.J., Sztarker, J. & Rind, F.C. (2013) . Looming detection by identified visual interneurons during larval development of the locust Locusta migratoria. Journal of Experimental Biology, 216(12), 2266-2275.
http://dx.doi.org/10.1242/jeb.083360
---------- CHICAGO ----------
Simmons, P.J., Sztarker, J., Rind, F.C. "Looming detection by identified visual interneurons during larval development of the locust Locusta migratoria" . Journal of Experimental Biology 216, no. 12 (2013) : 2266-2275.
http://dx.doi.org/10.1242/jeb.083360
---------- MLA ----------
Simmons, P.J., Sztarker, J., Rind, F.C. "Looming detection by identified visual interneurons during larval development of the locust Locusta migratoria" . Journal of Experimental Biology, vol. 216, no. 12, 2013, pp. 2266-2275.
http://dx.doi.org/10.1242/jeb.083360
---------- VANCOUVER ----------
Simmons, P.J., Sztarker, J., Rind, F.C. Looming detection by identified visual interneurons during larval development of the locust Locusta migratoria. J. Exp. Biol. 2013;216(12):2266-2275.
http://dx.doi.org/10.1242/jeb.083360