Literature DB >> 32839324

Mechanism for analogous illusory motion perception in flies and humans.

Margarida Agrochao1, Ryosuke Tanaka2, Emilio Salazar-Gatzimas2, Damon A Clark3,2,4,5.   

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.

Entities:  

Keywords:  Drosophila; neural circuits; peripheral drift illusion; vision

Mesh:

Year:  2020        PMID: 32839324      PMCID: PMC7502748          DOI: 10.1073/pnas.2002937117

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  65 in total

1.  The peripheral drift illusion: a motion illusion in the visual periphery.

Authors:  J Faubert; A M Herbert
Journal:  Perception       Date:  1999       Impact factor: 1.490

2.  Analogous motion illusion in man and fly.

Authors:  H Bülthoff; K G Götz
Journal:  Nature       Date:  1979-04-12       Impact factor: 49.962

3.  Directionally selective calcium signals in dendrites of starburst amacrine cells.

Authors:  Thomas Euler; Peter B Detwiler; Winfried Denk
Journal:  Nature       Date:  2002-08-04       Impact factor: 49.962

4.  Microsaccades and blinks trigger illusory rotation in the "rotating snakes" illusion.

Authors:  Jorge Otero-Millan; Stephen L Macknik; Susana Martinez-Conde
Journal:  J Neurosci       Date:  2012-04-25       Impact factor: 6.167

5.  Functional specialization of parallel motion detection circuits in the fly.

Authors:  Maximilian Joesch; Franz Weber; Hubert Eichner; Alexander Borst
Journal:  J Neurosci       Date:  2013-01-16       Impact factor: 6.167

6.  Spatial and temporal frequency selectivity of neurones in visual cortical areas V1 and V2 of the macaque monkey.

Authors:  K H Foster; J P Gaska; M Nagler; D A Pollen
Journal:  J Physiol       Date:  1985-08       Impact factor: 5.182

7.  Defining the computational structure of the motion detector in Drosophila.

Authors:  Damon A Clark; Limor Bursztyn; Mark A Horowitz; Mark J Schnitzer; Thomas R Clandinin
Journal:  Neuron       Date:  2011-06-23       Impact factor: 17.173

8.  Neural basis for a powerful static motion illusion.

Authors:  Bevil R Conway; Akiyoshi Kitaoka; Arash Yazdanbakhsh; Christopher C Pack; Margaret S Livingstone
Journal:  J Neurosci       Date:  2005-06-08       Impact factor: 6.709

9.  A common directional tuning mechanism of Drosophila motion-sensing neurons in the ON and in the OFF pathway.

Authors:  Juergen Haag; Abhishek Mishra; Alexander Borst
Journal:  Elife       Date:  2017-08-22       Impact factor: 8.140

10.  Do fish perceive illusory motion?

Authors:  Simone Gori; Christian Agrillo; Marco Dadda; Angelo Bisazza
Journal:  Sci Rep       Date:  2014-09-23       Impact factor: 4.379

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  8 in total

1.  Excitatory and inhibitory neural dynamics jointly tune motion detection.

Authors:  Aneysis D Gonzalez-Suarez; Jacob A Zavatone-Veth; Juyue Chen; Catherine A Matulis; Bara A Badwan; Damon A Clark
Journal:  Curr Biol       Date:  2022-07-21       Impact factor: 10.900

Review 2.  Illusional Perspective across Humans and Bees.

Authors:  Elia Gatto; Olli J Loukola; Maria Elena Miletto Petrazzini; Christian Agrillo; Simone Cutini
Journal:  Vision (Basel)       Date:  2022-05-31

3.  Shallow neural networks trained to detect collisions recover features of visual loom-selective neurons.

Authors:  Baohua Zhou; Zifan Li; Sunnie Kim; John Lafferty; Damon A Clark
Journal:  Elife       Date:  2022-01-13       Impact factor: 8.140

4.  Identifying Inputs to Visual Projection Neurons in Drosophila Lobula by Analyzing Connectomic Data.

Authors:  Ryosuke Tanaka 田中涼介; Damon A Clark
Journal:  eNeuro       Date:  2022-04-21

5.  From Receptive to Perceptive Fields: Size-Dependent Asymmetries in Both Negative Afterimages and Subcortical On and Off Post-Stimulus Responses.

Authors:  Xu Liu; Hui Li; Ye Wang; Tianhao Lei; Jijun Wang; Lothar Spillmann; Ian Max Andolina; Wei Wang
Journal:  J Neurosci       Date:  2021-07-29       Impact factor: 6.167

6.  Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit.

Authors:  Jennifer Ding; Albert Chen; Janet Chung; Hector Acaron Ledesma; Mofei Wu; David M Berson; Stephanie E Palmer; Wei Wei
Journal:  Elife       Date:  2021-06-07       Impact factor: 8.140

7.  Predicting individual neuron responses with anatomically constrained task optimization.

Authors:  Omer Mano; Matthew S Creamer; Bara A Badwan; Damon A Clark
Journal:  Curr Biol       Date:  2021-07-28       Impact factor: 10.900

8.  Motion illusion-like patterns extracted from photo and art images using predictive deep neural networks.

Authors:  Taisuke Kobayashi; Akiyoshi Kitaoka; Manabu Kosaka; Kenta Tanaka; Eiji Watanabe
Journal:  Sci Rep       Date:  2022-03-10       Impact factor: 4.379

  8 in total

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