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A Target-Detecting Visual Neuron in the Dragonfly Locks on to Selectively Attended Targets

Lancer, Benjamin H. ; Evans, Bernard J.E. LU ; Fabian, Joseph M. LU ; O'Carroll, David C. LU and Wiederman, Steven D. LU (2019) In The Journal of neuroscience : the official journal of the Society for Neuroscience 39(43). p.8497-8509
Abstract

The visual world projects a complex and rapidly changing image onto the retina of many animal species. This presents computational challenges for those animals reliant on visual processing to provide an accurate representation of the world. One such challenge is parsing a visual scene for the most salient targets, such as the selection of prey amid a swarm. The ability to selectively prioritize processing of some stimuli over others is known as 'selective attention'. We recently identified a dragonfly visual neuron called 'Centrifugal Small Target Motion Detector 1' (CSTMD1) that exhibits selective attention when presented with multiple, equally salient targets. Here we conducted in vivo, electrophysiological recordings from CSTMD1 in... (More)

The visual world projects a complex and rapidly changing image onto the retina of many animal species. This presents computational challenges for those animals reliant on visual processing to provide an accurate representation of the world. One such challenge is parsing a visual scene for the most salient targets, such as the selection of prey amid a swarm. The ability to selectively prioritize processing of some stimuli over others is known as 'selective attention'. We recently identified a dragonfly visual neuron called 'Centrifugal Small Target Motion Detector 1' (CSTMD1) that exhibits selective attention when presented with multiple, equally salient targets. Here we conducted in vivo, electrophysiological recordings from CSTMD1 in wild-caught male dragonflies (Hemicordulia tau), while presenting visual stimuli on an LCD monitor. To identify the target selected in any given trial, we uniquely modulated the intensity of the moving targets (frequency tagging). We found that the frequency information of the selected target is preserved in the neuronal response, while the distracter is completely ignored. We also show that the competitive system that underlies selection in this neuron can be biased by the presentation of a preceding target on the same trajectory, even when it is of lower contrast than an abrupt, novel distracter. With this improved method for identifying and biasing target selection in CSTMD1, the dragonfly provides an ideal animal model system to probe the neuronal mechanisms underlying selective attention.SIGNIFICANCE STATEMENT We present the first application of frequency tagging to intracellular neuronal recordings, demonstrating that the frequency component of a stimulus is encoded in the spiking response of an individual neuron. Using this technique as an identifier, we demonstrate that CSTMD1 'locks on' to a selected target and encodes the absolute strength of this target, even in the presence of abruptly appearing, high-contrast distracters. The underlying mechanism also permits the selection mechanism to switch between targets mid-trial, even among equivalent targets. Together, these results demonstrate greater complexity in this selective attention system than would be expected in a winner-takes-all network. These results are in contrast to typical findings in the primate and avian brain, but display intriguing resemblance to observations in human psychophysics.

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author
; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
insect vision, predictive gain modulation, priming, selective attention, target detection, winner-takes-all
in
The Journal of neuroscience : the official journal of the Society for Neuroscience
volume
39
issue
43
pages
13 pages
publisher
Society for Neuroscience
external identifiers
  • pmid:31519823
ISSN
1529-2401
DOI
10.1523/JNEUROSCI.1431-19.2019
language
English
LU publication?
yes
id
58d5adf3-9db1-4805-889d-04b4d2c3fcd2
date added to LUP
2019-11-05 13:59:59
date last changed
2020-05-10 06:44:28
@article{58d5adf3-9db1-4805-889d-04b4d2c3fcd2,
  abstract     = {<p>The visual world projects a complex and rapidly changing image onto the retina of many animal species. This presents computational challenges for those animals reliant on visual processing to provide an accurate representation of the world. One such challenge is parsing a visual scene for the most salient targets, such as the selection of prey amid a swarm. The ability to selectively prioritize processing of some stimuli over others is known as 'selective attention'. We recently identified a dragonfly visual neuron called 'Centrifugal Small Target Motion Detector 1' (CSTMD1) that exhibits selective attention when presented with multiple, equally salient targets. Here we conducted in vivo, electrophysiological recordings from CSTMD1 in wild-caught male dragonflies (Hemicordulia tau), while presenting visual stimuli on an LCD monitor. To identify the target selected in any given trial, we uniquely modulated the intensity of the moving targets (frequency tagging). We found that the frequency information of the selected target is preserved in the neuronal response, while the distracter is completely ignored. We also show that the competitive system that underlies selection in this neuron can be biased by the presentation of a preceding target on the same trajectory, even when it is of lower contrast than an abrupt, novel distracter. With this improved method for identifying and biasing target selection in CSTMD1, the dragonfly provides an ideal animal model system to probe the neuronal mechanisms underlying selective attention.SIGNIFICANCE STATEMENT We present the first application of frequency tagging to intracellular neuronal recordings, demonstrating that the frequency component of a stimulus is encoded in the spiking response of an individual neuron. Using this technique as an identifier, we demonstrate that CSTMD1 'locks on' to a selected target and encodes the absolute strength of this target, even in the presence of abruptly appearing, high-contrast distracters. The underlying mechanism also permits the selection mechanism to switch between targets mid-trial, even among equivalent targets. Together, these results demonstrate greater complexity in this selective attention system than would be expected in a winner-takes-all network. These results are in contrast to typical findings in the primate and avian brain, but display intriguing resemblance to observations in human psychophysics.</p>},
  author       = {Lancer, Benjamin H. and Evans, Bernard J.E. and Fabian, Joseph M. and O'Carroll, David C. and Wiederman, Steven D.},
  issn         = {1529-2401},
  language     = {eng},
  number       = {43},
  pages        = {8497--8509},
  publisher    = {Society for Neuroscience},
  series       = {The Journal of neuroscience : the official journal of the Society for Neuroscience},
  title        = {A Target-Detecting Visual Neuron in the Dragonfly Locks on to Selectively Attended Targets},
  url          = {http://dx.doi.org/10.1523/JNEUROSCI.1431-19.2019},
  doi          = {10.1523/JNEUROSCI.1431-19.2019},
  volume       = {39},
  year         = {2019},
}