Distributed Dendritic Processing Facilitates Object Detection: A Computational Analysis on the Visual System of the Fly
Hennig P, Möller R, Egelhaaf M (2008)
PLoS ONE 3(8): e3092.
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Background: Detecting objects is an important task when moving through a natural environment. Flies, for example, may land on salient objects or may avoid collisions with them. The neuronal ensemble of Figure Detection cells (FD-cells) in the visual system of the fly is likely to be involved in controlling these behaviours, as these cells are more sensitive to objects than to extended background structures. Until now the computations in the presynaptic neuronal network of FD-cells and, in particular, the functional significance of the experimentally established distributed dendritic processing of excitatory and inhibitory inputs is not understood. Methodology/Principal Findings: We use model simulations to analyse the neuronal computations responsible for the preference of FD-cells for small objects. We employed a new modelling approach which allowed us to account for the spatial spread of electrical signals in the dendrites while avoiding detailed compartmental modelling. The models are based on available physiological and anatomical data. Three models were tested each implementing an inhibitory neural circuit, but differing by the spatial arrangement of the inhibitory interaction. Parameter optimisation with an evolutionary algorithm revealed that only distributed dendritic processing satisfies the constraints arising from electrophysiological experiments. In contrast to a direct dendro-dendritic inhibition of the FD-cell (Direct Distributed Inhibition model), an inhibition of its presynaptic retinotopic elements (Indirect Distributed Inhibition model) requires smaller changes in input resistance in the inhibited neurons during visual stimulation. Conclusions/Significance: Distributed dendritic inhibition of retinotopic elements as implemented in our Indirect Distributed Inhibition model is the most plausible wiring scheme for the neuronal circuit of FD-cells. This microcircuit is computationally similar to lateral inhibition between the retinotopic elements. Hence, distributed inhibition might be an alternative explanation of perceptual phenomena currently explained by lateral inhibition networks.
Erscheinungsjahr
2008
Zeitschriftentitel
PLoS ONE
Band
3
Ausgabe
8
Art.-Nr.
e3092
ISSN
1932-6203
Page URI
https://pub.uni-bielefeld.de/record/1936829
Zitieren
Hennig P, Möller R, Egelhaaf M. Distributed Dendritic Processing Facilitates Object Detection: A Computational Analysis on the Visual System of the Fly. PLoS ONE. 2008;3(8): e3092.
Hennig, P., Möller, R., & Egelhaaf, M. (2008). Distributed Dendritic Processing Facilitates Object Detection: A Computational Analysis on the Visual System of the Fly. PLoS ONE, 3(8), e3092. https://doi.org/10.1371/journal.pone.0003092
Hennig, Patrick, Möller, Ralf, and Egelhaaf, Martin. 2008. “Distributed Dendritic Processing Facilitates Object Detection: A Computational Analysis on the Visual System of the Fly”. PLoS ONE 3 (8): e3092.
Hennig, P., Möller, R., and Egelhaaf, M. (2008). Distributed Dendritic Processing Facilitates Object Detection: A Computational Analysis on the Visual System of the Fly. PLoS ONE 3:e3092.
Hennig, P., Möller, R., & Egelhaaf, M., 2008. Distributed Dendritic Processing Facilitates Object Detection: A Computational Analysis on the Visual System of the Fly. PLoS ONE, 3(8): e3092.
P. Hennig, R. Möller, and M. Egelhaaf, “Distributed Dendritic Processing Facilitates Object Detection: A Computational Analysis on the Visual System of the Fly”, PLoS ONE, vol. 3, 2008, : e3092.
Hennig, P., Möller, R., Egelhaaf, M.: Distributed Dendritic Processing Facilitates Object Detection: A Computational Analysis on the Visual System of the Fly. PLoS ONE. 3, : e3092 (2008).
Hennig, Patrick, Möller, Ralf, and Egelhaaf, Martin. “Distributed Dendritic Processing Facilitates Object Detection: A Computational Analysis on the Visual System of the Fly”. PLoS ONE 3.8 (2008): e3092.
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7 Zitationen in Europe PMC
Daten bereitgestellt von Europe PubMed Central.
Dendritic end inhibition in large-field visual neurons of the fly.
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PMID: 23426692
Elyada YM, Haag J, Borst A., J Neurosci 33(8), 2013
PMID: 23426692
Monitoring of single-cell responses in the optic tectum of adult zebrafish with dextran-coupled calcium dyes delivered via local electroporation.
Kassing V, Engelmann J, Kurtz R., PLoS One 8(5), 2013
PMID: 23667529
Kassing V, Engelmann J, Kurtz R., PLoS One 8(5), 2013
PMID: 23667529
Object representation and distance encoding in three-dimensional environments by a neural circuit in the visual system of the blowfly.
Liang P, Heitwerth J, Kern R, Kurtz R, Egelhaaf M., J Neurophysiol 107(12), 2012
PMID: 22423002
Liang P, Heitwerth J, Kern R, Kurtz R, Egelhaaf M., J Neurophysiol 107(12), 2012
PMID: 22423002
Neuronal encoding of object and distance information: a model simulation study on naturalistic optic flow processing.
Hennig P, Egelhaaf M., Front Neural Circuits 6(), 2012
PMID: 22461769
Hennig P, Egelhaaf M., Front Neural Circuits 6(), 2012
PMID: 22461769
Spatial vision in insects is facilitated by shaping the dynamics of visual input through behavioral action.
Egelhaaf M, Boeddeker N, Kern R, Kurtz R, Lindemann JP., Front Neural Circuits 6(), 2012
PMID: 23269913
Egelhaaf M, Boeddeker N, Kern R, Kurtz R, Lindemann JP., Front Neural Circuits 6(), 2012
PMID: 23269913
Binocular integration of visual information: a model study on naturalistic optic flow processing.
Hennig P, Kern R, Egelhaaf M., Front Neural Circuits 5(), 2011
PMID: 21519385
Hennig P, Kern R, Egelhaaf M., Front Neural Circuits 5(), 2011
PMID: 21519385
Localized direction selective responses in the dendrites of visual interneurons of the fly.
Spalthoff C, Egelhaaf M, Tinnefeld P, Kurtz R., BMC Biol 8(), 2010
PMID: 20384983
Spalthoff C, Egelhaaf M, Tinnefeld P, Kurtz R., BMC Biol 8(), 2010
PMID: 20384983
53 References
Daten bereitgestellt von Europe PubMed Central.
Visual receptive fields in the superior colliculus of the cat.
Sterling P, Wickelgren BG., J. Neurophysiol. 32(1), 1969
PMID: 5765229
Sterling P, Wickelgren BG., J. Neurophysiol. 32(1), 1969
PMID: 5765229
Influence of the presentation of remote visual stimuli on visual responses of cat area 17 and lateral suprasylvian area.
Rizzolatti G, Camarda R., Exp Brain Res 29(1), 1977
PMID: 891678
Rizzolatti G, Camarda R., Exp Brain Res 29(1), 1977
PMID: 891678
Responsiveness of cells in the cat's superior colliculus to textured visual stimuli.
Mason R., Exp Brain Res 37(2), 1979
PMID: 499388
Mason R., Exp Brain Res 37(2), 1979
PMID: 499388
Double-opponent-process mechanism underlying RF-structure of directionally specific cells of cat lateral suprasylvian visual area.
von Grunau M, Frost BJ., Exp Brain Res 49(1), 1983
PMID: 6305699
von Grunau M, Frost BJ., Exp Brain Res 49(1), 1983
PMID: 6305699
Responses of visual cells in cat superior colliculus to relative pattern movement.
Mandl G., Vision Res. 25(2), 1985
PMID: 4013093
Mandl G., Vision Res. 25(2), 1985
PMID: 4013093
Direction- and velocity-specific responses from beyond the classical receptive field in the middle temporal visual area (MT).
Allman J, Miezin F, McGuinness E., Perception 14(2), 1985
PMID: 4069941
Allman J, Miezin F, McGuinness E., Perception 14(2), 1985
PMID: 4069941
Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey.
Tanaka K, Hikosaka K, Saito H, Yukie M, Fukada Y, Iwai E., J. Neurosci. 6(1), 1986
PMID: 3944614
Tanaka K, Hikosaka K, Saito H, Yukie M, Fukada Y, Iwai E., J. Neurosci. 6(1), 1986
PMID: 3944614
Selectivity for relative motion in the monkey superior colliculus.
Davidson RM, Bender DB., J. Neurophysiol. 65(5), 1991
PMID: 1869908
Davidson RM, Bender DB., J. Neurophysiol. 65(5), 1991
PMID: 1869908
Moving background patterns reveal double-opponency of directionally specific pigeon tectal neurons.
Frost BJ, Scilley PL, Wong SC., Exp Brain Res 43(2), 1981
PMID: 7250263
Frost BJ, Scilley PL, Wong SC., Exp Brain Res 43(2), 1981
PMID: 7250263
Deep tectal cells in pigeons respond to kinematograms.
Frost BJ, Cavanagh P, Morgan B., 1988
Frost BJ, Cavanagh P, Morgan B., 1988
Single visual neurons code opposing motion independent of direction.
Frost BJ, Nakayama K., Science 220(4598), 1983
PMID: 6836313
Frost BJ, Nakayama K., Science 220(4598), 1983
PMID: 6836313
Response of toad's tectal neurons to in-phase and anti-phase movements of object and textured background.
Tsai HJ., 1990
Tsai HJ., 1990
Neuronal basis of a sensory analyser, the acridid movement detector system. III. Control of response amplitude by tonic lateral inhibition.
Fraser Rowell CH, O'Shea M., J. Exp. Biol. 65(3), 1976
PMID: 1018165
Fraser Rowell CH, O'Shea M., J. Exp. Biol. 65(3), 1976
PMID: 1018165
The neuronal basis of a sensory analyser, the acridid movement detector system. IV. The preference for small field stimuli.
Fraser Rowell CH, O'Shea M, Williams JL., J. Exp. Biol. 68(), 1977
PMID: 894184
Fraser Rowell CH, O'Shea M, Williams JL., J. Exp. Biol. 68(), 1977
PMID: 894184
Vision during flight
Collett TS, King AJ., 1975
Collett TS, King AJ., 1975
Visual Neurones in the Anterior Optic Tract of the Privet Hawk Moth.
Collett TS., 1972
Collett TS., 1972
Object- and self-movement detectors in the ventral nerve cord of the dragonfly.
Olberg RM., 1981
Olberg RM., 1981
Identified target-selective visual interneurons descending from the dragonfly brain.
Olberg RM., 1986
Olberg RM., 1986
Feature-detecting neurons in dragonflies.
O'Carroll DC., 1993
O'Carroll DC., 1993
On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. II. Figure-detection cells a new class of visual interneurones.
Egelhaaf M., 1985
Egelhaaf M., 1985
Spatial response properties of contralateral inhibited lobula plate tangential cells in the fly visual system.
Gauck V, Borst A., J. Comp. Neurol. 406(1), 1999
PMID: 10100892
Gauck V, Borst A., J. Comp. Neurol. 406(1), 1999
PMID: 10100892
Retinotopic organization of small-field-target-detecting neurons in the insect visual system.
Barnett PD, Nordstrom K, O'carroll DC., Curr. Biol. 17(7), 2007
PMID: 17363248
Barnett PD, Nordstrom K, O'carroll DC., Curr. Biol. 17(7), 2007
PMID: 17363248
Neural mechanisms underlying target detection in a dragonfly centrifugal neuron.
Geurten BR, Nordstrom K, Sprayberry JD, Bolzon DM, O'Carroll DC., J. Exp. Biol. 210(Pt 18), 2007
PMID: 17766305
Geurten BR, Nordstrom K, Sprayberry JD, Bolzon DM, O'Carroll DC., J. Exp. Biol. 210(Pt 18), 2007
PMID: 17766305
On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. III. Possible input circuitries and behavioural significance of the FD-cells.
Egelhaaf M., 1985
Egelhaaf M., 1985
Detection of object motion by a fly neuron during simulated flight.
Kimmerle B, Egelhaaf M., 2000
Kimmerle B, Egelhaaf M., 2000
Objekt detection in the fly during simulated translatory flight.
Kimmerle B, Warzecha AK, Egelhaaf M., 1997
Kimmerle B, Warzecha AK, Egelhaaf M., 1997
Neural circuit tuning fly visual interneurons to motion of small objects. I. Dissection of the circuit by pharmacological and photoinactivation techniques.
Warzecha AK, Egelhaaf M, Borst A., J. Neurophysiol. 69(2), 1993
PMID: 8459270
Warzecha AK, Egelhaaf M, Borst A., J. Neurophysiol. 69(2), 1993
PMID: 8459270
Figure-Ground Discrimination by Relative Movement in the Visual System of the fly. Part II: Towards the Neural Circuitry.
Reichardt W, Poggio T, Hausen K., 1983
Reichardt W, Poggio T, Hausen K., 1983
Processing of synaptic signals in fly visual interneurons selectively responsive to small moving objects
Borst A, Egelhaaf M., 1993
Borst A, Egelhaaf M., 1993
Dendro-dendritic interactions between motion-sensitive large-field neurons in the fly.
Haag J, Borst A., J. Neurosci. 22(8), 2002
PMID: 11943823
Haag J, Borst A., J. Neurosci. 22(8), 2002
PMID: 11943823
Neural circuit tuning fly visual neurons to motion of small objects. II. Input organization of inhibitory circuit elements revealed by electrophysiological and optical recording techniques.
Egelhaaf M, Borst A, Warzecha AK, Flecks S, Wildemann A., J. Neurophysiol. 69(2), 1993
PMID: 8459271
Egelhaaf M, Borst A, Warzecha AK, Flecks S, Wildemann A., J. Neurophysiol. 69(2), 1993
PMID: 8459271
An elaborated model of fly small-target tracking.
Higgins CM, Pant V., Biol Cybern 91(6), 2004
PMID: 15597180
Higgins CM, Pant V., Biol Cybern 91(6), 2004
PMID: 15597180
Neural image processing by dendritic networks.
Cuntz H, Haag J, Borst A., Proc. Natl. Acad. Sci. U.S.A. 100(19), 2003
PMID: 12947039
Cuntz H, Haag J, Borst A., Proc. Natl. Acad. Sci. U.S.A. 100(19), 2003
PMID: 12947039
Koch C, Segev I., 1998
Motion sensitive interneurons in the optomotor system of the fly. I. The Horizontal Cells: Structure and signals
Hausen K., 1982
Hausen K., 1982
Motion sensitive interneurons in the optomotor system of the fly. II. The Horizontal Cells: Receptive field organization and response characteristics.
Hausen K., 1982
Hausen K., 1982
The neural computation of visual motion
Egelhaaf M., 2006
Egelhaaf M., 2006
Functional charaterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowfly Calliphora erythrocephala.
Hausen K., 1976
Hausen K., 1976
Synapse distribution on VCH, an inhibitory, motion-sensitive interneuron in the fly visual system.
Gauck V, Egelhaaf M, Borst A., J. Comp. Neurol. 381(4), 1997
PMID: 9136805
Gauck V, Egelhaaf M, Borst A., J. Comp. Neurol. 381(4), 1997
PMID: 9136805
Koch C., 1999
On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly. I. Behavioural constraints imposed on the neuronal network and the role of the optomotor system.
Egelhaaf M., 1985
Egelhaaf M., 1985
Membrane potential fluctuations determine the precision of spike timing and synchronous activity: a model study.
Kretzberg J, Egelhaaf M, Warzecha AK., J Comput Neurosci 10(1), 2001
PMID: 11316342
Kretzberg J, Egelhaaf M, Warzecha AK., J Comput Neurosci 10(1), 2001
PMID: 11316342
An introduction to differential evolution
Price KV., 1999
Price KV., 1999
Struktur, Funktion und Konnektivität bewegungsempfindlicher Interneurone im dritten optischen Neuropil der Schmeissfliege Calliphora erythrocephala.
Hausen K., 1976
Hausen K., 1976
Intracellular staining of insect neurons with procion yellow
Hengstenberg R, Hengstenberg B., 1980
Hengstenberg R, Hengstenberg B., 1980
Dendritic computation of direction selectivity and gain control in visual interneurons.
Single S, Haag J, Borst A., J. Neurosci. 17(16), 1997
PMID: 9236213
Single S, Haag J, Borst A., J. Neurosci. 17(16), 1997
PMID: 9236213
Implications of functionally different synaptic inputs for neuronal gain and computational properties of fly visual interneurons.
Grewe J, Matos N, Egelhaaf M, Warzecha AK., J. Neurophysiol. 96(4), 2006
PMID: 16790602
Grewe J, Matos N, Egelhaaf M, Warzecha AK., J. Neurophysiol. 96(4), 2006
PMID: 16790602
Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing.
Koch C, Poggio T, Torre V., Proc. Natl. Acad. Sci. U.S.A. 80(9), 1983
PMID: 6573680
Koch C, Poggio T, Torre V., Proc. Natl. Acad. Sci. U.S.A. 80(9), 1983
PMID: 6573680
Binocular contributions to optic flow processing in the fly visual system.
Krapp HG, Hengstenberg R, Egelhaaf M., J. Neurophysiol. 85(2), 2001
PMID: 11160507
Krapp HG, Hengstenberg R, Egelhaaf M., J. Neurophysiol. 85(2), 2001
PMID: 11160507
Movement detection in arthropods.
Egelhaaf M, Borst A., 1993
Egelhaaf M, Borst A., 1993
Über die Wirkung der räumlichen Vertheilung des Lichtreizes auf der Netzhaut, I Sitzungsberichte der mathematisch-naturwissenschaftlichen Classe der kaiserlichen Akademie der Wissenschaften
Mach E., 1865
Mach E., 1865
Békésy G., 1967
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