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Abstract:

Highly active insects and crabs depend on visual motion information for detecting and tracking mates, prey, or predators, for which they require directional control systems containing internal maps of visual space. A neural map formed by large, motion-sensitive neurons implicated in processing panoramic flow is known to exist in an optic ganglion of the fly. However, an equivalent map for processing spatial positions of single objects has not been hitherto identified in any arthropod. Crabs can escape directly away from a visual threat wherever the stimulus is located in the 360° field of view. When tested in a walking simulator, the crab Neohelice granulata immediately adjusts its running direction after changes in the position of the visual danger stimulus smaller than 1°. Combining mass and single-cell staining with in vivo intracellular recording, we show that a particular class of motion-sensitive neurons of the crab's lobula that project to the midbrain, the monostratified lobula giants type 1 (MLG1), form a system of 16 retinotopically organized elements that map the 360° azimuthal space. The preference of these neurons for horizontally moving objects conforms the visual ecology of the crab's mudflat world. With a mean receptive field of 118°, MLG1s have a large superposition among neighboring elements. Our results suggest that the MLG1 system conveys information on object position as a population vector. Such computational code can enable the accurate directional control observed in the visually guided behaviors of crabs. © 2015 the authors.

Registro:

Documento: Artículo
Título:A network of visual motion-sensitive neurons for computing object position in an arthropod
Autor:Medan, V.; De Astrada, M.B.; Scarano, F.; Tomsic, D.
Filiación:Instituto de Fisiología, Biología Molecular y Neurociencias-Concejo Nacional de Investigaciones Científicas y Tecnológicas, Departamento de Fisiología, Biología Molecular y Celular, Universidad de Buenos Aires, Buenos Aires, 1428, Argentina
Palabras clave:Cell ensemble; Crab; Escape direction; Giant lobula neurons; Insect; Population coding; adult; animal experiment; animal model; animal tissue; arthropod; Article; behavior; brain electrophysiology; computer analysis; connectome; controlled study; correlation coefficient; eye movement; habituation; male; morphological trait; motion analysis system; neuroanatomy; nonhuman; priority journal; retina receptive field; sensory nerve; visual stimulation; action potential; animal; Brachyura; cytology; escape behavior; in vitro study; movement (physiology); movement perception; nerve cell network; normal distribution; optic lobe; orientation; physiology; sensory nerve cell; visual field; visual system; Action Potentials; Animals; Brachyura; Escape Reaction; In Vitro Techniques; Male; Motion Perception; Movement; Nerve Net; Normal Distribution; Optic Lobe, Nonmammalian; Orientation; Sensory Receptor Cells; Visual Fields; Visual Pathways
Año:2015
Volumen:35
Número:17
Página de inicio:6654
Página de fin:6666
DOI: http://dx.doi.org/10.1523/JNEUROSCI.4667-14.2015
Título revista:Journal of Neuroscience
Título revista abreviado:J. Neurosci.
ISSN:02706474
CODEN:JNRSD
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02706474_v35_n17_p6654_Medan

Referencias:

  • Barnes, W.J.P., Nalbach, H.-O., Eye movements in freely moving crabs: Their sensory basis and possible role in flow-field analysis (1993) Comparative Biochemistry and Physiology Part A: Physiology, 104, pp. 675-693
  • 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. , CrossRef Medline
  • 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. , CrossRef Medline
  • 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. , CrossRef Medline
  • Berón de Astrada, M., Bengochea, M., Sztarker, J., Delorenzi, A., Tomsic, D., Behaviorally related neural plasticity in the arthropod optic lobes (2013) Curr Biol, 23, pp. 1389-1398. , CrossRef Medline
  • Borst, A., Fly visual course control: Behaviour, algorithms and circuits (2014) Nat Rev Neurosci, 15, pp. 590-599. , CrossRef Medline
  • Borst, A., Weber, F., Neural action fields for optic flow based naviga-tion: A simulation study of the fly lobula plate network (2011) PLoS One, 6. , CrossRef Medline
  • Dewell, R.B., Gabbiani, F., Escape behavior: Linking neural computation to action (2012) Curr Biol, 22, pp. R152-R153. , CrossRef Medline
  • 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. , CrossRef Medline
  • Georgopoulos, A.P., Schwartz, A.B., Kettner, R.E., Neuronal population coding of movement direction (1986) Science, 233, pp. 1416-1419. , CrossRef Medline
  • Gonzalez-Bellido, P.T., Peng, H., Yang, J., Georgopoulos, A.P., Olberg, R.M., Eight pairs of descending visual neurons in the dragonfly give wing motor centers accurate population vector of prey direction (2013) Proc Natl Acad Sci USA, 110, pp. 696-701. , CrossRef Medline
  • Gronenberg, W., Strausfeld, N.J., Descending pathways connecting the male-specific visual system of flies to the neck and flight motor (1991) J Comp Physiol A, 169, pp. 413-426. , Medline
  • Heinze, S., Homberg, U., Map like representation of celestial E-vector orientations in the brain of an insect (2007) Science, 315, pp. 995-997. , CrossRef Medline
  • 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. , CrossRef Medline
  • Karmeier, K., Krapp, H.G., Egelhaaf, M., Population coding of self-mo-tion: Applying bayesian analysis to a population of visual interneurons in the fly (2005) J Neurophysiol, 94, pp. 2182-2194. , CrossRef Medline
  • Kuffler, S.W., Discharge patterns and functional organization of mammalian retina (1953) J Neurophysiol, 16, pp. 37-68. , Medline
  • 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. , CrossRef
  • Lennie, P., Single units and visual cortical organization (1998) Perception, 27, pp. 889-935. , CrossRef Medline
  • Levi, R., Camhi, J.M., Population vector coding by the giant interneurons of the cockroach (2000) J Neurosci, 20, pp. 3822-3829. , Medline
  • Lewis, J.E., Kristan, W.B., Jr., A neuronal network for computing population vectors in the leech (1998) Nature, 391, pp. 76-79. , CrossRef Medline
  • Lindemann, J.P., Egelhaaf, M., Texture dependence of motion sensing and free flight behavior in blowflies (2012) Front Behav Neurosci 6:92, , Medline
  • 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. , CrossRef Medline
  • Nalbach, H.-O., Visually elicited escape in crabs (1990) Frontiers in crustacean neurobiology, pp. 165-172. , (Wiese K, Krent WD, Tautz J, Reichert H, Mulloney B, eds). Basel: Birkhauser Verlag
  • Nordstrom, K., Barnett, P.D., O'Carroll, D.C., Insect detection of small targets moving in visual clutter (2006) PLoS Biol, 4. , CrossRef Medline
  • 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. , CrossRef Medline
  • Oliva, D., Tomsic, D., Computation of object approach by a system of visual motion-sensitive neurons in the crab Neohelice (2014) J Neurophysiol, 112, pp. 1477-1490. , CrossRef Medline
  • Oliva, D., Medan, V., Tomsic, D., Escape behavior and neuronal responses to looming stimuli in the crab Chasmagnathus granulatus (Deca-poda: Grapsidae) (2007) J Exp Biol, 210, pp. 865-880. , CrossRef Medline
  • Rosner, R., Homberg, U., Widespread sensitivity to looming stimuli and small moving objects in the central complex of an insect brain (2013) J Neurosci, 33, pp. 8122-8133. , CrossRef Medline
  • Salzman, C.D., Newsome, W.T., Neural mechanisms for forming a perceptual decision (1994) Science, 264, pp. 231-237. , CrossRef Medline
  • Scarano, F., Tomsic, D., Escape response of the crab Neohelice to computer generated looming and translational visual danger stimuli (2014) J Physiol Paris, 108, pp. 141-147. , CrossRef Medline
  • Silies, M., Gohl, D.M., Clandinin, T.R., Motion-detecting circuits in flies: Coming into view (2014) Annu Rev Neurosci, 37, pp. 307-327. , CrossRef Medline
  • Simmons, P.J., Connexions between a movement-detecting visual interneurone and flight motoneurones of a locust (1980) J Exp Biol, 86, pp. 87-97
  • Strausfeld, N.J., Structural organization of male-specific visual neurons in calliphorid optic lobes (1991) J Comp Physiol A, 169, pp. 379-393. , Medline
  • Strausfeld, N.J., Brain organization and the origin of insects: An assessment (2009) Proc Biol Sci, 276, pp. 1929-1937. , CrossRef Medline
  • 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. , Medline
  • 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. , CrossRef Medline
  • Sztarker, J., Tomsic, D., Brain modularity in arthropods: Individual neurons that support "what" but not "where" memories (2011) J Neurosci, 31, pp. 8175-8180. , CrossRef Medline
  • 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. , CrossRef Medline
  • Tomsic, D., Berón de Astrada, M., Sztarker, J., Identification of individual neurons reflecting short-and long-term visual memory in an arthro-podo (2003) J Neurosci, 23, pp. 8539-8546. , Medline
  • Trischler, C., Boeddeker, N., Egelhaaf, M., Characterisation of a blowfly male-specific neuron using behaviourally generated visual stimuli (2007) J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 193, pp. 559-572. , CrossRef Medline
  • Trousdale, J., Carroll, S.R., Gabbiani, F., Josić, K., Near-optimal decoding of transient stimuli from coupled neuronal subpopulations (2014) J Neurosci, 34, pp. 12206-12222. , CrossRef Medline
  • Zeil, J., Al-Mutairi, M., The variation of resolution and of ommatidial dimensions in the compound eyes of the fiddler crab Uca lactea annulipes (Ocypodidae, Brachyura, Decapoda) (1996) J Exp Biol, 199, pp. 1569-1577. , Medline
  • Zeil, J., Zanker, J.M., A glimpse into crabworld (1997) Vision Res, 37, pp. 3417-3426. , CrossRef Medline
  • Zeil, J., Nalbach, G., Nalbach, H.-O., Spatial vision in a flat world: Optical and neural adaptations in arthropods (1989) Neurobiology of sensory systems, pp. 123-137. , (Singh RN, Strausfeld NJ, eds). New York: Springer

Citas:

---------- APA ----------
Medan, V., De Astrada, M.B., Scarano, F. & Tomsic, D. (2015) . A network of visual motion-sensitive neurons for computing object position in an arthropod. Journal of Neuroscience, 35(17), 6654-6666.
http://dx.doi.org/10.1523/JNEUROSCI.4667-14.2015
---------- CHICAGO ----------
Medan, V., De Astrada, M.B., Scarano, F., Tomsic, D. "A network of visual motion-sensitive neurons for computing object position in an arthropod" . Journal of Neuroscience 35, no. 17 (2015) : 6654-6666.
http://dx.doi.org/10.1523/JNEUROSCI.4667-14.2015
---------- MLA ----------
Medan, V., De Astrada, M.B., Scarano, F., Tomsic, D. "A network of visual motion-sensitive neurons for computing object position in an arthropod" . Journal of Neuroscience, vol. 35, no. 17, 2015, pp. 6654-6666.
http://dx.doi.org/10.1523/JNEUROSCI.4667-14.2015
---------- VANCOUVER ----------
Medan, V., De Astrada, M.B., Scarano, F., Tomsic, D. A network of visual motion-sensitive neurons for computing object position in an arthropod. J. Neurosci. 2015;35(17):6654-6666.
http://dx.doi.org/10.1523/JNEUROSCI.4667-14.2015