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Properties of predictive gain modulation in a dragonfly visual neuron

Fabian, Joseph M. LU ; Dunbier, James R. ; O'Carroll, David C. LU and Wiederman, Steven D. LU (2019) In The Journal of experimental biology 222.
Abstract

Dragonflies pursue and capture tiny prey and conspecifics with extremely high success rates. These moving targets represent a small visual signal on the retina and successful chases require accurate detection and amplification by downstream neuronal circuits. This amplification has been observed in a population of neurons called small target motion detectors (STMDs), through a mechanism we term predictive gain modulation. As targets drift through the neuron's receptive field, spike frequency builds slowly over time. This increased likelihood of spiking or gain is modulated across the receptive field, enhancing sensitivity just ahead of the target's path, with suppression of activity in the remaining surround. Whilst some properties of... (More)

Dragonflies pursue and capture tiny prey and conspecifics with extremely high success rates. These moving targets represent a small visual signal on the retina and successful chases require accurate detection and amplification by downstream neuronal circuits. This amplification has been observed in a population of neurons called small target motion detectors (STMDs), through a mechanism we term predictive gain modulation. As targets drift through the neuron's receptive field, spike frequency builds slowly over time. This increased likelihood of spiking or gain is modulated across the receptive field, enhancing sensitivity just ahead of the target's path, with suppression of activity in the remaining surround. Whilst some properties of this mechanism have been described, it is not yet known which stimulus parameters modulate the amount of response gain. Previous work suggested that the strength of gain enhancement was predominantly determined by the duration of the target's prior path. Here, we show that predictive gain modulation is more than a slow build-up of responses over time. Rather, the strength of gain is dependent on the velocity of a prior stimulus combined with the current stimulus attributes (e.g. angular size). We also describe response variability as a major challenge of target-detecting neurons and propose that the role of predictive gain modulation is to drive neurons towards response saturation, thus minimising neuronal variability despite noisy visual input signals.

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author
; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Insect vision, Neuronal facilitation, Receptive field, Small target motion detector
in
The Journal of experimental biology
volume
222
article number
jeb207316
publisher
The Company of Biologists Ltd
external identifiers
  • pmid:31395677
  • scopus:85071831540
ISSN
1477-9145
DOI
10.1242/jeb.207316
language
English
LU publication?
yes
id
65e377e7-1a58-4d42-9509-28db648ee324
date added to LUP
2019-09-16 14:39:01
date last changed
2024-04-16 19:58:36
@article{65e377e7-1a58-4d42-9509-28db648ee324,
  abstract     = {{<p>Dragonflies pursue and capture tiny prey and conspecifics with extremely high success rates. These moving targets represent a small visual signal on the retina and successful chases require accurate detection and amplification by downstream neuronal circuits. This amplification has been observed in a population of neurons called small target motion detectors (STMDs), through a mechanism we term predictive gain modulation. As targets drift through the neuron's receptive field, spike frequency builds slowly over time. This increased likelihood of spiking or gain is modulated across the receptive field, enhancing sensitivity just ahead of the target's path, with suppression of activity in the remaining surround. Whilst some properties of this mechanism have been described, it is not yet known which stimulus parameters modulate the amount of response gain. Previous work suggested that the strength of gain enhancement was predominantly determined by the duration of the target's prior path. Here, we show that predictive gain modulation is more than a slow build-up of responses over time. Rather, the strength of gain is dependent on the velocity of a prior stimulus combined with the current stimulus attributes (e.g. angular size). We also describe response variability as a major challenge of target-detecting neurons and propose that the role of predictive gain modulation is to drive neurons towards response saturation, thus minimising neuronal variability despite noisy visual input signals.</p>}},
  author       = {{Fabian, Joseph M. and Dunbier, James R. and O'Carroll, David C. and Wiederman, Steven D.}},
  issn         = {{1477-9145}},
  keywords     = {{Insect vision; Neuronal facilitation; Receptive field; Small target motion detector}},
  language     = {{eng}},
  publisher    = {{The Company of Biologists Ltd}},
  series       = {{The Journal of experimental biology}},
  title        = {{Properties of predictive gain modulation in a dragonfly visual neuron}},
  url          = {{http://dx.doi.org/10.1242/jeb.207316}},
  doi          = {{10.1242/jeb.207316}},
  volume       = {{222}},
  year         = {{2019}},
}