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Research Article

Mechanism for analogous illusory motion perception in flies and humans

View ORCID ProfileMargarida Agrochao, View ORCID ProfileRyosuke Tanaka, Emilio Salazar-Gatzimas, and View ORCID ProfileDamon A. Clark
PNAS September 15, 2020 117 (37) 23044-23053; first published August 24, 2020; https://doi.org/10.1073/pnas.2002937117
Margarida Agrochao
aDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511;
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  • ORCID record for Margarida Agrochao
Ryosuke Tanaka
bInterdepartmental Neuroscience Program, Yale University, New Haven, CT 06511;
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Emilio Salazar-Gatzimas
bInterdepartmental Neuroscience Program, Yale University, New Haven, CT 06511;
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Damon A. Clark
aDepartment of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT 06511;
bInterdepartmental Neuroscience Program, Yale University, New Haven, CT 06511;
cDepartment of Physics, Yale University, New Haven, CT 06511;
dDepartment of Neuroscience, Yale University, New Haven, CT 06511
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  • For correspondence: damon.clark@yale.edu
  1. Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved July 13, 2020 (received for review March 1, 2020)

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Significance

Most of the time, visual circuitry in our brains faithfully reports visual scenes. Sometimes, however, it can report motion in images that are in fact stationary, leading us to perceive illusory motion. In this study, we establish that fruit flies, too, perceive motion in the stationary images that evoke illusory motion in humans. Our results demonstrate how this motion illusion in flies is an artifact of the brain’s strategies for efficiently processing motion in natural scenes. Perceptual tests in humans suggest that our brains may employ similar mechanisms for this illusion. This study shows how illusions can provide insight into visual processing mechanisms and principles across phyla.

Abstract

Visual motion detection is one of the most important computations performed by visual circuits. Yet, we perceive vivid illusory motion in stationary, periodic luminance gradients that contain no true motion. This illusion is shared by diverse vertebrate species, but theories proposed to explain this illusion have remained difficult to test. Here, we demonstrate that in the fruit fly Drosophila, the illusory motion percept is generated by unbalanced contributions of direction-selective neurons’ responses to stationary edges. First, we found that flies, like humans, perceive sustained motion in the stationary gradients. The percept was abolished when the elementary motion detector neurons T4 and T5 were silenced. In vivo calcium imaging revealed that T4 and T5 neurons encode the location and polarity of stationary edges. Furthermore, our proposed mechanistic model allowed us to predictably manipulate both the magnitude and direction of the fly’s illusory percept by selectively silencing either T4 or T5 neurons. Interestingly, human brains possess the same mechanistic ingredients that drive our model in flies. When we adapted human observers to moving light edges or dark edges, we could manipulate the magnitude and direction of their percepts as well, suggesting that mechanisms similar to the fly’s may also underlie this illusion in humans. By taking a comparative approach that exploits Drosophila neurogenetics, our results provide a causal, mechanistic account for a long-known visual illusion. These results argue that this illusion arises from architectures for motion detection that are shared across phyla.

  • vision
  • Drosophila
  • neural circuits
  • peripheral drift illusion

Footnotes

  • ↵1M.A. and R.T. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. Email: damon.clark{at}yale.edu.
  • Author contributions: M.A., R.T., E.S.-G., and D.A.C. designed research; M.A., R.T., and E.S.-G. performed research; M.A., R.T., E.S.-G., and D.A.C. analyzed data; and M.A., R.T., and D.A.C. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2002937117/-/DCSupplemental.

Data Availability.

Detailed materials and methods are reported in SI Appendix. All experimental data are available in Dryad (https://doi.org/10.5061/dryad.vt4b8gtpd), and scripts to analyze the data and run the computational models are available in GitHub (https://github.com/ClarkLabCode/IllusionPaperCode).

Published under the PNAS license.

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Mechanism for analogous illusory motion perception in flies and humans
Margarida Agrochao, Ryosuke Tanaka, Emilio Salazar-Gatzimas, Damon A. Clark
Proceedings of the National Academy of Sciences Sep 2020, 117 (37) 23044-23053; DOI: 10.1073/pnas.2002937117

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Mechanism for analogous illusory motion perception in flies and humans
Margarida Agrochao, Ryosuke Tanaka, Emilio Salazar-Gatzimas, Damon A. Clark
Proceedings of the National Academy of Sciences Sep 2020, 117 (37) 23044-23053; DOI: 10.1073/pnas.2002937117
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Proceedings of the National Academy of Sciences: 117 (37)
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