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


For many animals, the visual detection of looming stimuli is crucial at any stage of their lives. For example, human babies of only 6 days old display evasive responses to looming stimuli (Bower et al. [1971]: Percept Psychophys 9: 193-196). This means the neuronal pathways involved in looming detection should mature early in life. Locusts have been used extensively to examine the neural circuits and mechanisms involved in sensing looming stimuli and triggering visually evoked evasive actions, making them ideal subjects in which to investigate the development of looming sensitivity. Two lobula giant movement detectors (LGMD) neurons have been identified in the lobula region of the locust visual system: the LGMD1 neuron responds selectively to looming stimuli and provides information that contributes to evasive responses such as jumping and emergency glides. The LGMD2 responds to looming stimuli and shares many response properties with the LGMD1. Both neurons have only been described in the adult. In this study, we describe a practical method combining classical staining techniques and 3D neuronal reconstructions that can be used, even in small insects, to reveal detailed anatomy of individual neurons. We have used it to analyze the anatomy of the fan-shaped dendritic tree of the LGMD1 and the LGMD2 neurons in all stages of the post-embryonic development of Locusta migratoria. We also analyze changes seen during the ontogeny of escape behaviors triggered by looming stimuli, specially the hiding response. © 2014 Wiley Periodicals, Inc.


Documento: Artículo
Título:A look into the cockpit of the developing locust: Looming detectors and predator avoidance
Autor: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, IFIBYNE-CONICET, Pabellon 2 Ciudad Universitaria, Intendente Guiraldes 2160, Buenos Aires, 1428, Argentina
Palabras clave:Development; Hiding; LGMD; Looming detection; Neuronal reconstruction; age; animal; Caelifera; confocal microscopy; escape behavior; female; growth, development and aging; larva; male; nerve cell; perceptive discrimination; photostimulation; physiology; three dimensional imaging; visual system; Age Factors; Animals; Escape Reaction; Female; Grasshoppers; Imaging, Three-Dimensional; Larva; Male; Microscopy, Confocal; Neurons; Photic Stimulation; Signal Detection, Psychological; Visual Pathways
Página de inicio:1078
Página de fin:1095
Título revista:Developmental Neurobiology
Título revista abreviado:Dev. Neurobiol.


  • 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
  • Anton, S., Ignell, R., Hansson, B.S., Developmental changes in the structure and function of the central olfactory system in gregarious and solitary desert locusts (2002) Microsc Res Tech, 56, pp. 281-291
  • Barth, M., Hirsch, H.V., Meinertzhagen, I.A., Heisenberg, M., Experience-dependent developmental plasticity in the optic lobe of Drosophila melanogaster (1997) J Neurosci, 17, pp. 1493-1504
  • Bastiani, M., Pearson, K.G., Goodman, C.S., From embryonic fascicles to adult tracts: Organization of neuropile from a developmental perspective (1984) J Exp Biol, 112, pp. 45-64
  • Bentley, D., Toroian-Raymond, A., Embryonic and postembryonic morphogenesis of a grasshopper interneuron (1981) J Comp Neurol, 201, pp. 507-518
  • Bentley, D.R., Hoy, R.R., Postembryonic development of adult motor patterns in crickets: A neural analysis (1970) Science, 170, pp. 1409-1411
  • Blagburn, J.M., Beadle, D.J., Morphology of identified cercal afferents and giant interneurones in the hatchling cockroach Periplaneta americana (1982) J Exp Biol, 97, pp. 421-426
  • Bower, T.G.R., Broughton, J.M., Moore, M.K., Infant responses to approaching objects: An indicator of response to distal variables (1971) Percept Psychophys, 9, pp. 193-196
  • 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., Directional sensitivity of an identified wind-sensitive interneuron during the postembryonic development of the locust (2000) J Insect Physiol, 46, pp. 1545-1556
  • Consoulas, C., Duch, C., Bayline, R.J., Levine, R.B., Behavioral transformations during metamorphosis: Remodeling of neural and motor systems (2000) Brain Res Bull, 53, pp. 571-583
  • Dagan, D., Volman, S., Sensory basis for directional wind detection in first instar cockroaches, Periplaneta americana (1982) J Comp Physiol, 147, pp. 471-478
  • Fotowat, H., Fayyazuddin, A., Bellen, H.J., Gabbiani, F., A novel neuronal pathway for visually guided escape in Drosophila melanogaster (2009) J Neurophysiol, 102, pp. 875-885
  • 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., Gabbiani, F., Collision detection as a model for sensory-motor integration (2011) Annu Rev Neurosci, 34, pp. 1-19
  • 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
  • Gabbiani, F., Krapp, H.G., Koch, C., Laurent, G., Multiplicative computation in a visual neuron sensitive to looming (2002) Nature, 420, pp. 320-324
  • 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
  • Heisinger, P.R., Zhai, R.G., Zhou, Y., Koh, T.W., Mehta, S.Q., Schulze, K.L., Cao, Y., Bellen, H.J., Activity-independent prespecification of synaptic partners in the visual map of Drosophila (2006) Curr Biol, 16, pp. 1835-1843
  • Hammond, S., O'Shea, M., Ontogeny of flight initiation in the fly Drosophila melanogaster: Implications for the giant fibre system (2007) J Comp Physiol A, 193, pp. 1125-1137
  • Hassenstein, B., Hustert, R., Hiding responses of locusts to approaching objects (1999) J Exp Biol, 202, pp. 1701-1710
  • Hatsopoulos, N., Gabbiani, F., Laurent, G., Elementary computation of object approach by wide-field visual neuron (1995) Science, 270, pp. 1000-1003
  • 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
  • Leitch, B., Shepherd, D., Laurent, G., Morphogenesis of the branching pattern of a group of spiking local interneurons in relation to the organisation of embryonic sensory neuropils in locust (1995) Philos Trans R Soc London B, 349, pp. 433-447
  • Libersat, F., Duch, C., Morphometric analysis of dendritic remodeling in an identified motoneuron during postembryonic development (2002) J Comp Neurol, 450, pp. 153-166
  • Meinertzhagen, I.A., The organization of perpendicular fibre pathways in the insect optic lobe (1976) Philos Trans R Soc London B, 274, pp. 555-594
  • Meseke, M., Evers, J.F., Duch, C., Developmental changes in dendritic shape and synapse location tune single-neuron computations to changing behavioral functions (2009) J Neurophysiol, 102, pp. 41-58
  • Nakagawa, H., Hongjian, K., Collision-sensitive neurons in the optic tectum of the bullfrog, Rana catesbeiana (2010) J Neurophysiol, 104, pp. 2487-2499
  • O'Shea, M., Williams, J.L.D., The anatomy and output connection of a locust visual interneurone; the lobular giant movement detector (LGMD) neurone (1974) J Comp Physiol, 91, pp. 257-266
  • 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
  • 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
  • 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
  • Raper, J.A., Bastiani, M., Goodman, C.S., Pathfinding by neuronal growth cones in grasshopper embryos (1983) I. Divergent choices made by the growth cones of sibling neurons. J Neurosci, 3, pp. 20-30
  • Raper, J.A., Bastiani, M., Goodman, C.S., Pathfinding by neuronal growth cones in grasshopper embryos (1983) II. Selective fasciculation onto specific axonal pathways. J Neurosci, 3, pp. 31-41
  • Rencher, A.C., Interpretation of canonical discriminant functions, canonical variates, and principal components (1992) Am Stat, 46, pp. 217-225
  • 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., Non-directional, movement sensitive neurones of the locust optic lobe (1987) J Comp Physiol, 161, pp. 477-494
  • Rind, F.C., Intracellular characterization of neurons in the locust brain signaling impending collision (1996) J Neurophysiol, 75, pp. 986-995
  • 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., Santer, R.D., Collision avoidance and a looming sensitive neuron: Size matters but biggest is not necessarily best (2004) Proc Biol Sci, 271, pp. S27-S29
  • Rind, F.C., Simmons, P.J., Orthopteran DCMD neuron: A reevaluation of responses to moving objects (1992) I. Selective responses to approaching objects. 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
  • Rowell, C.H.F., The orthopteran descending movement detector (DMD) neurones: A characterisation and review (1971) Z Vergl Physiol, 73, pp. 167-194
  • Rybak, J., Meinertzhagen, I.A., The effects of light reversals on photoreceptor synaptogenesis in the fly Musca domestica (1997) Eur J Neurosci, 9, pp. 319-333
  • 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., Simmons, P.J., Rind, F.C., Gliding behaviour elicited by lateral looming stimuli in flying locusts (2005) J Comp Physiol A, 191, pp. 61-73
  • 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
  • Schlotterer, G.R., 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
  • Shankland, M., Goodman, C.S., Development of the dendritic branching pattern of the medial giant interneuron in the grasshopper embryo (1982) Dev Biol, 92, pp. 489-506
  • Simmons, P.J., Rind, F.C., Orthopteran DCMD neuron: A reevaluation of responses to moving objects (1992) II. Critical cues for detecting approaching objects. 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
  • 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
  • Stevenson, P.A., Kutsch, W., Basic circuitry of an adult-specific motor program completed with embryogenesis (1986) Naturwissenschaften, 73, pp. 741-743
  • 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
  • Sztarker, J., Strausfeld, N.J., Tomsic, D., Organization of optic lobes that support motion detection in a semiterrestrial crab (2005) J Comp Neurol, 493, pp. 396-411
  • Wright, G.A., Lutmerding, A., Dudareva, N., Smith, B.H., Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera) (2005) J Comp Physiol A, 191, pp. 105-114


---------- APA ----------
Sztarker, J. & Rind, F.C. (2014) . A look into the cockpit of the developing locust: Looming detectors and predator avoidance. Developmental Neurobiology, 74(11), 1078-1095.
---------- CHICAGO ----------
Sztarker, J., Rind, F.C. "A look into the cockpit of the developing locust: Looming detectors and predator avoidance" . Developmental Neurobiology 74, no. 11 (2014) : 1078-1095.
---------- MLA ----------
Sztarker, J., Rind, F.C. "A look into the cockpit of the developing locust: Looming detectors and predator avoidance" . Developmental Neurobiology, vol. 74, no. 11, 2014, pp. 1078-1095.
---------- VANCOUVER ----------
Sztarker, J., Rind, F.C. A look into the cockpit of the developing locust: Looming detectors and predator avoidance. Dev. Neurobiol. 2014;74(11):1078-1095.