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Modeling Nonlinear Dendritic Processing of Facilitation in a Dragonfly Target-Tracking Neuron

Bekkouche, Bo M.B. LU ; Shoemaker, Patrick A. ; Fabian, Joseph M. LU ; Rigosi, Elisa LU ; Wiederman, Steven D. LU and O’Carroll, David C. LU (2021) In Frontiers in Neural Circuits 15.
Abstract

Dragonflies are highly skilled and successful aerial predators that are even capable of selectively attending to one target within a swarm. Detection and tracking of prey is likely to be driven by small target motion detector (STMD) neurons identified from several insect groups. Prior work has shown that dragonfly STMD responses are facilitated by targets moving on a continuous path, enhancing the response gain at the present and predicted future location of targets. In this study, we combined detailed morphological data with computational modeling to test whether a combination of dendritic morphology and nonlinear properties of NMDA receptors could explain these observations. We developed a hybrid computational model of neurons within... (More)

Dragonflies are highly skilled and successful aerial predators that are even capable of selectively attending to one target within a swarm. Detection and tracking of prey is likely to be driven by small target motion detector (STMD) neurons identified from several insect groups. Prior work has shown that dragonfly STMD responses are facilitated by targets moving on a continuous path, enhancing the response gain at the present and predicted future location of targets. In this study, we combined detailed morphological data with computational modeling to test whether a combination of dendritic morphology and nonlinear properties of NMDA receptors could explain these observations. We developed a hybrid computational model of neurons within the dragonfly optic lobe, which integrates numerical and morphological components. The model was able to generate potent facilitation for targets moving on continuous trajectories, including a localized spotlight of maximal sensitivity close to the last seen target location, as also measured during in vivo recordings. The model did not, however, include a mechanism capable of producing a traveling or spreading wave of facilitation. Our data support a strong role for the high dendritic density seen in the dragonfly neuron in enhancing non-linear facilitation. An alternative model based on the morphology of an unrelated type of motion processing neuron from a dipteran fly required more than three times higher synaptic gain in order to elicit similar levels of facilitation, despite having only 20% fewer synapses. Our data support a potential role for NMDA receptors in target tracking and also demonstrate the feasibility of combining biologically plausible dendritic computations with more abstract computational models for basic processing as used in earlier studies.

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author
; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
BSTMD1, dragonfly, facilitation, insect brain, lobula, NMDA, small target motion detector, STMD
in
Frontiers in Neural Circuits
volume
15
article number
684872
publisher
Frontiers Media S. A.
external identifiers
  • pmid:34483847
  • scopus:85114229744
ISSN
1662-5110
DOI
10.3389/fncir.2021.684872
language
English
LU publication?
yes
id
0d119edf-d96a-42e3-b6ac-c9df1b402f42
date added to LUP
2021-10-05 15:02:55
date last changed
2024-06-15 17:29:50
@article{0d119edf-d96a-42e3-b6ac-c9df1b402f42,
  abstract     = {{<p>Dragonflies are highly skilled and successful aerial predators that are even capable of selectively attending to one target within a swarm. Detection and tracking of prey is likely to be driven by small target motion detector (STMD) neurons identified from several insect groups. Prior work has shown that dragonfly STMD responses are facilitated by targets moving on a continuous path, enhancing the response gain at the present and predicted future location of targets. In this study, we combined detailed morphological data with computational modeling to test whether a combination of dendritic morphology and nonlinear properties of NMDA receptors could explain these observations. We developed a hybrid computational model of neurons within the dragonfly optic lobe, which integrates numerical and morphological components. The model was able to generate potent facilitation for targets moving on continuous trajectories, including a localized spotlight of maximal sensitivity close to the last seen target location, as also measured during in vivo recordings. The model did not, however, include a mechanism capable of producing a traveling or spreading wave of facilitation. Our data support a strong role for the high dendritic density seen in the dragonfly neuron in enhancing non-linear facilitation. An alternative model based on the morphology of an unrelated type of motion processing neuron from a dipteran fly required more than three times higher synaptic gain in order to elicit similar levels of facilitation, despite having only 20% fewer synapses. Our data support a potential role for NMDA receptors in target tracking and also demonstrate the feasibility of combining biologically plausible dendritic computations with more abstract computational models for basic processing as used in earlier studies.</p>}},
  author       = {{Bekkouche, Bo M.B. and Shoemaker, Patrick A. and Fabian, Joseph M. and Rigosi, Elisa and Wiederman, Steven D. and O’Carroll, David C.}},
  issn         = {{1662-5110}},
  keywords     = {{BSTMD1; dragonfly; facilitation; insect brain; lobula; NMDA; small target motion detector; STMD}},
  language     = {{eng}},
  month        = {{08}},
  publisher    = {{Frontiers Media S. A.}},
  series       = {{Frontiers in Neural Circuits}},
  title        = {{Modeling Nonlinear Dendritic Processing of Facilitation in a Dragonfly Target-Tracking Neuron}},
  url          = {{http://dx.doi.org/10.3389/fncir.2021.684872}},
  doi          = {{10.3389/fncir.2021.684872}},
  volume       = {{15}},
  year         = {{2021}},
}