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Abstract:

Similar to most visual animals, crabs perform proper avoidance responses to objects directly approaching them. The monostratified lobula giant neurons of type 1 (MLG1) of crabs constitute an ensemble of 14–16 bilateral pairs of motion-detecting neurons projecting from the lobula (third optic neuropile) to the midbrain, with receptive fields that are distributed over the extensive visual field of the animal’s eye. Considering the crab Neohelice (previously Chasmagnathus) granulata, here we describe the response of these neurons to looming stimuli that simulate objects approaching the animal on a collision course. We found that the peak firing time of MLG1 acts as an angular threshold detector signaling, with a delay of δ = 35 ms, the time at which an object reaches a fixed angular threshold of 49°. Using in vivo intracellular recordings, we detected the existence of excitatory and inhibitory synaptic currents that shape the neural response. Other functional features identified in the MLG1 neurons were phasic responses at the beginning of the approach, a relation between the stimulus angular velocity and the excitation delay, and a mapping between membrane potential and firing frequency. Using this information, we propose a biophysical model of the mechanisms that regulate the encoding of looming stimuli. Furthermore, we found that the parameter encoded by the MLG1 firing frequency during the approach is the stimulus angular velocity. The proposed model fits the experimental results and predicts the neural response to a qualitatively different stimulus. Based on these and previous results, we propose that the MLG1 neuron system acts as a directional coding system for collision avoidance. © 2014 the American Physiological Society.

Registro:

Documento: Artículo
Título:Computation of object approach by a system of visual motion-sensitive neurons in the crab Neohelice
Autor:Oliva, D.; Tomsic, D.
Filiación:Departamento de Ciencia y Tecnología, Universidad Nacional de Quilmes, CONICET, Buenos Aires, Argentina
Laboratorio de Neurobiología de la Memoria, Departamento Fisiología Biología Molecular y Celular, Universidad de Buenos Aires, IFIBYNE-CONICET, Buenos Aires, Argentina
Palabras clave:Collision avoidance; Crustacean; Lobula neurons; Looming; Motion detection; Receptive field; adult; animal behavior; animal cell; animal experiment; Article; avoidance behavior; crab; giant nerve cell; in vivo study; intracellular recording; latent period; male; monostratified lobula giant neuron type 1; Neohelice granulata; nerve cell membrane potential; nerve cell stimulation; neurotransmission; nonhuman; sensory nerve cell; stimulus response; synaptic transmission; animal; biological model; Brachyura; cytology; excitatory postsynaptic potential; inhibitory postsynaptic potential; membrane potential; mesencephalon; movement perception; neuropil; physiology; reaction time; sensory nerve cell; visual field; Animals; Brachyura; Excitatory Postsynaptic Potentials; Inhibitory Postsynaptic Potentials; Membrane Potentials; Mesencephalon; Models, Neurological; Motion Perception; Neurons, Afferent; Neuropil; Reaction Time; Visual Fields
Año:2014
Volumen:112
Número:6
Página de inicio:1477
Página de fin:1490
DOI: http://dx.doi.org/10.1152/jn.00921.2013
Título revista:Journal of Neurophysiology
Título revista abreviado:J. Neurophysiol.
ISSN:00223077
CODEN:JONEA
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00223077_v112_n6_p1477_Oliva

Referencias:

  • Berón De Astrada, M., Tomsic, D., Physiology and morphology of visual movement detector neurons in a crab (decapoda: Brachyura) (2002) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 188, pp. 539-551
  • Berón De Astrada, M., Medan, V., Tomsic, D., How visual space maps in the optic neuropils of a crab (2011) J Comp Neurol, 519, pp. 1631-1639
  • Berón De Astrada, M., Bengochea, M., Medan, V., Tomsic, D., Regionalization in the eye of the grapsid crab neohelice granulata (chasmagnathus granulatus): Variation of resolution and facet diameters (2012) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 198, pp. 173-180
  • Borst, A., Fly visual interneurons responsive to image expansion (1991) Zool Jb Physiol, 95, pp. 305-313
  • Card, G.M., Escape behaviors in insects (2012) Curr Opin Neurob, 22, pp. 180-186
  • Chan, R.W., Gabbiani, F., Collision-avoidance behaviors of minimally restrained flying locusts to looming stimuli (2013) J Exp Biol, 216, pp. 641-655
  • Destexhe, A., Mainen, Z.F., Sejnowski, T.J., An efficient method for computing synaptic conductances based on a kinetic model of receptor binding (1994) Neural Comput, 6, pp. 14-18
  • 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
  • Gabbiani, F., Mo, C., Laurent, G., Invariance of angular threshold computation in a wide-field looming sensitive neuron (2001) J Neurosci, 21, pp. 314-329
  • Gabbiani, F., Krapp, H.G., Koch, C., Laurent, G., Multiplicative computation in a visual neuron sensitive to looming (2002) Nature, 21, pp. 320-324
  • 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
  • Glantz, R.M., Defense reflex and motion detector responsiveness to approaching targets: The motion detector trigger to the defense reflex pathway (1974) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 95, pp. 297-314
  • Glantz, R.M., Habituation of the motion detectors of the crayfish optic nerve: Their relationship to the visually evoked defense reflex (1974) J Neurobiol, 5, pp. 489-510
  • Gray, J.R., Habituated visual neurons in locusts remain sensitive to novel looming objects (2005) J Exp Biol, 208, pp. 2515-2532
  • 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 Neuroethol Sens Neural Behav Physiol, 196, pp. 927-938
  • Herberholz, J., Marquart, G., Decision making and behavioral choice during predator avoidance (2012) Front Neurosci, 6, pp. 1-15
  • Hemmi, J.M., Predator avoidance in fiddler crabs: 1. Escape decisions in relation to the risk of predation (2005) Animal Behav, 69, pp. 603-614
  • Hemmi, J.M., Predator avoidance in fiddler crabs: 2. The visual cues (2005) Animal Behav, 69, pp. 615-625
  • Hemmi, J.M., Tomsic, D., The neuroethology of escape in crabs: From sensory ecology to neurons and back (2012) Curr Opin Neurobiol, 22, pp. 194-200
  • Iribarne, O.O., Martinez, M.M., Predation on the southwestern atlantic fiddler crab (uca uruguayensis) by migratory shorebirds (pluvialis dominica, p. Squatarola, arenaria interpres, and numenius phaeopus) (1999) Estuaries, 22, pp. 47-54
  • Jones, P.W., Gabbiani, F., Synchronized neural input shapes stimulus selectivity in a collision-detecting neuron (2010) Curr Biol, 20, pp. 2052-2057
  • 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
  • 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
  • Land, M., Layne, J., The visual control of behaviour in fiddler crabs (1995) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 177, pp. 91-103
  • Laughlin, S.B., Hardie, R.C., Comon strategies for light adaptation in the peripheral visual systems of fly and dragonfly (1978) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 128, pp. 319-340
  • Layne, J., Wicklein, M., Dodge, F.A., Barlow, R.B., Prediction of maximum allowable retinal slip speed in the fiddler crab, uca pugilator (1997) Biol Bull, 193, pp. 202-203
  • McMillan, G.A., Loessin, V., Gray, J.R., Bilateral flight muscle activity predicts wing kinematics and 3-dimensional body orientation of locusts responding to looming objects (2013) J Exp Biol, 216, pp. 3369-3380
  • Medan, V., Oliva, D., Tomsic, D., Characterization of lobula giant neurons responsive to visual stimuli that elicit escape behaviors in the crab chasmagnathus (2007) J Neurophysiol, 98, pp. 2414-2428
  • Medan, V., (2008) Caracterización Morfológico-Funcional De Neuronas Sensibles Al Movimiento Involucradas En Comportamientos Visuales Del Cangrejo Chasmagnathus, , http://digital.bl.fcen.uba.ar/Download/Tesis/Tesis_4323_Medan.pdf, (PhD Thesis). Buenos Aires, Argentina: Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires
  • Nalbach, H.O., Visually elicited escape in crabs (1990) Frontiers in Crustacean Neurobiology, , edited by Wiese K, Krenz WD, Tautz J, Reichert H, Mulloney B. Basel, Switzerland: Basel
  • Oliva, D., Medan, V., Tomsic, D., Escape behavior and neuronal responses to looming stimuli in the crab chasmagnathus granulatus (2007) J Exp Biol, 210, pp. 865-880. , (Decapoda: Grapsidae)
  • Oliva, D., Mecanismos de detección visual y evitación de colisiones en un nuevo modelo experimental, el cangrejo chasmagnathus granulatus (2010) Buenos Aires, , http://digital.bl.fcen.uba.ar/Download/Tesis/Tesis_4678_Oliva.pdf, (On-line), Argentina: Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires
  • Oliva, D., Tomsic, D., Visuo-motor transformations involved in the escape response to looming stimuli in the crab neohelice (chasmagnathus) granulata (2012) J Exp Biol, 215, pp. 3488-3500
  • Oliva, D., Collision avoidance models (2013) Encyclopedia of Computational Neuroscience: Springerreference, , edited by Jaeger D, Jung R. Berlin, Heidelberg: Springer-Verlag
  • O’Shea, M., Rowell, C.H., Protection from habituation by lateral inhibition (1975) Nature, 254, pp. 53-55
  • Peron, S.P., Gabbiani, F., Spike frequency adaptation mediates looming stimulus selectivity in a collision detecting neuron (2009) Nat Neurosci, 12, pp. 318-326
  • Rind, F.C., Non-directional, movement sensitive neurons of the locust optic lobe (1987) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 161, pp. 477-494
  • 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., 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., Simmons, P.J., Seeing what is coming: Building collision sensitive neurones (1999) Trends Neurosci, 22, pp. 215-220
  • Rowell, C.H., 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., Simmons, P.J., Rind, F.C., Gliding behaviour elicited by lateral looming stimuli in flying locusts (2005) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 191, pp. 61-73
  • Santer, R.D., Yamawaki, Y., Rind, F.C., Simmons, P.J., Motor activity and trajectory control during escape jumping in the locust locusta migratoria (2005) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 191, pp. 965-975
  • 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
  • Srinivasan, M.V., Zhang, S., Visual motor computations in insects (2004) Annu Rev Neurosci, 27, pp. 679-696
  • Strausfeld, N.J., The evolution of crustacean and insect optic lobes and the origins of chiasmata (2005) Arthropod Struct Dev, 34, pp. 235-256
  • Sztarker, J., Tomsic, D., Binocular visual integration in the crustacean nervous system (2004) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 190, pp. 951-962
  • 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
  • Sztarker, J., Tomsic, D., Neuronal correlates of the visually elicited escape response of the crab chasmagnathus upon seasonal variations, stimuli changes and perceptual alterations (2008) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 194, pp. 587-596
  • Sztarker, J., Strausfeld, N., Andrew, D., Tomsic, D., Neural organization of first optic neuropils in the littoral crab hemigrapsus oregonensis and the semiterrestrial species chasmagnathus granulatus (2009) J Comp Neurol, 513, pp. 129-150
  • Sztarker, J., Tomsic, D., Brain modularity in arthropods: Individual neurons that support “what” but not “where” memories (2011) J Neurosci, 31, pp. 8175-8180
  • Tammero, L.F., Dickinson, M.H., Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly drosophila melanogaster (2002) J Exp Biol, 205, pp. 2785-2798
  • Tomsic, D., Berón De Astrada, M., Sztarker, J., Identification of individual neurons reflecting short- and long-term visual memory in an arthropod (2003) J Neurosci, 23, pp. 8539-8546
  • Wasserman, L., (2004) All of Statistics: A Concise Course in Statistical Inference, pp. 107-110. , Berlin, Heidelberg: Springer, chapt 8
  • Weber, F., Machens, C.K., Borst, A., Spatiotemporal response properties of optic-flow processing neurons (2010) Neuron, 67, pp. 629-642
  • Wiersma, C.A., Roach, J.L., Glantz, R.M., Neural integration in the optic system (1982) The Biology of the Crustacea, 4. , Neural Integration and Behavior, edited by Sandeman DC, Atwood HL. New York: Academic
  • Yamawaki, Y., Toh, Y., Response properties of visual interneurons to motion stimuli in the praying mantis, tenodera aridifolia (2003) Zool Sci, 20, pp. 819-832
  • Yamawaki, Y., Toh, Y., Responses of descending neurons to looming stimuli in the praying mantis tenodera aridifolia (2009) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 195, pp. 253-264

Citas:

---------- APA ----------
Oliva, D. & Tomsic, D. (2014) . Computation of object approach by a system of visual motion-sensitive neurons in the crab Neohelice. Journal of Neurophysiology, 112(6), 1477-1490.
http://dx.doi.org/10.1152/jn.00921.2013
---------- CHICAGO ----------
Oliva, D., Tomsic, D. "Computation of object approach by a system of visual motion-sensitive neurons in the crab Neohelice" . Journal of Neurophysiology 112, no. 6 (2014) : 1477-1490.
http://dx.doi.org/10.1152/jn.00921.2013
---------- MLA ----------
Oliva, D., Tomsic, D. "Computation of object approach by a system of visual motion-sensitive neurons in the crab Neohelice" . Journal of Neurophysiology, vol. 112, no. 6, 2014, pp. 1477-1490.
http://dx.doi.org/10.1152/jn.00921.2013
---------- VANCOUVER ----------
Oliva, D., Tomsic, D. Computation of object approach by a system of visual motion-sensitive neurons in the crab Neohelice. J. Neurophysiol. 2014;112(6):1477-1490.
http://dx.doi.org/10.1152/jn.00921.2013