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.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Abstract / Bemerkung
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.
Elyada YM, Haag J, Borst A., J Neurosci 33(8), 2013
PMID: 23426692
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
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
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

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
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
Selectivity for relative motion in the monkey superior colliculus.
Davidson RM, Bender DB., J. Neurophysiol. 65(5), 1991
PMID: 1869908
Deep tectal cells in pigeons respond to kinematograms.
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
Response of toad's tectal neurons to in-phase and anti-phase movements of object and textured background.
Tsai HJ., 1990
Vision during flight
Collett TS, King AJ., 1975
Visual neurones for tracking moving targets.
Collett T., Nature 232(5306), 1971
PMID: 4933247
Visual Neurones in the Anterior Optic Tract of the Privet Hawk Moth.
Collett TS., 1972
Object- and self-movement detectors in the ventral nerve cord of the dragonfly.
Olberg RM., 1981
Identified target-selective visual interneurons descending from the dragonfly brain.
Olberg RM., 1986
Feature-detecting neurons in dragonflies.
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
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
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
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
Detection of object motion by a fly neuron during simulated flight.
Kimmerle B, Egelhaaf M., 2000
Objekt detection in the fly during simulated translatory flight.
Kimmerle B, Warzecha AK, Egelhaaf M., 1997
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
Processing of synaptic signals in fly visual interneurons selectively responsive to small moving objects
Borst A, Egelhaaf M., 1993
An elaborated model of fly small-target tracking.
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

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
Motion sensitive interneurons in the optomotor system of the fly. II. The Horizontal Cells: Receptive field organization and response characteristics.
Hausen K., 1982
The neural computation of visual motion
Egelhaaf M., 2006
Functional charaterization and anatomical identification of motion sensitive neurons in the lobula plate of the blowfly Calliphora erythrocephala.
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

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
An introduction to differential evolution
Price KV., 1999
Struktur, Funktion und Konnektivität bewegungsempfindlicher Interneurone im dritten optischen Neuropil der Schmeissfliege Calliphora erythrocephala.
Hausen K., 1976
Intracellular staining of insect neurons with procion yellow
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
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
Binocular contributions to optic flow processing in the fly visual system.
Krapp HG, Hengstenberg R, Egelhaaf M., J. Neurophysiol. 85(2), 2001
PMID: 11160507
Movement detection in arthropods.
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

Békésy G., 1967
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