The Neuronal Basis of an Illusory Motion Percept Is Explained by Decorrelation of Parallel Motion Pathways

Potters, 1994, Statistical mechanics and visual signal processing, J. Phys. I France, 4, 1755, 10.1051/jp1:1994219 Fitzgerald, 2015, Nonlinear circuits for naturalistic visual motion estimation, eLife, 4, e09123, 10.7554/eLife.09123 Fitzgerald, 2011, Symmetries in stimulus statistics shape the form of visual motion estimators, Proc. Natl. Acad. Sci. USA, 108, 12909, 10.1073/pnas.1015680108 Borst, 2015, Common circuit design in fly and mammalian motion vision, Nat. Neurosci., 18, 1067, 10.1038/nn.4050 Clark, 2016, Parallel computations in insect and mammalian visual motion processing, Curr. Biol., 26, R1062, 10.1016/j.cub.2016.08.003 Hassenstein, 1956, Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus, Z. Naturforsch. B, 11, 513, 10.1515/znb-1956-9-1004 Anstis, 1970, Phi movement as a subtraction process, Vision Res., 10, 1411, 10.1016/0042-6989(70)90092-1 Orger, 2000, Perception of Fourier and non-Fourier motion by larval zebrafish, Nat. Neurosci., 3, 1128, 10.1038/80649 Livingstone, 2001, Two-dimensional substructure of MT receptive fields, Neuron, 30, 781, 10.1016/S0896-6273(01)00313-0 Bours, 2009, Sensitivity for reverse-phi motion, Vision Res., 49, 1, 10.1016/j.visres.2008.09.014 Clark, 2011, Defining the computational structure of the motion detector in Drosophila, Neuron, 70, 1165, 10.1016/j.neuron.2011.05.023 de Ruyter van Steveninck, R.R., Bialek, W., Potters, M., Carlson, R.H., and Lewen, G.D. (1994). Adaptive movement computation by the blowfly visual system. In Proceedings of the Fifth NEC Research Symposium. pp. 21–41. Leong, 2016, Direction selectivity in Drosophila emerges from preferred-direction enhancement and null-direction suppression, J. Neurosci., 36, 8078, 10.1523/JNEUROSCI.1272-16.2016 Borst, 2018, A biophysical mechanism for preferred direction enhancement in fly motion vision, PLoS Comput. Biol., 14, e1006240, 10.1371/journal.pcbi.1006240 Barlow, 1965, The mechanism of directionally selective units in rabbit’s retina, J. Physiol., 178, 477, 10.1113/jphysiol.1965.sp007638 Livingstone, 2003, Substructure of direction-selective receptive fields in macaque V1, J. Neurophysiol., 89, 2743, 10.1152/jn.00822.2002 Eichner, 2011, Internal structure of the fly elementary motion detector, Neuron, 70, 1155, 10.1016/j.neuron.2011.03.028 Joesch, 2013, Functional specialization of parallel motion detection circuits in the fly, J. Neurosci., 33, 902, 10.1523/JNEUROSCI.3374-12.2013 Maisak, 2013, A directional tuning map of Drosophila elementary motion detectors, Nature, 500, 212, 10.1038/nature12320 Buchner, 1984, Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement, J. Comp. Physiol. A, 155, 471, 10.1007/BF00611912 Tuthill, 2011, Neural correlates of illusory motion perception in Drosophila, Proc. Natl. Acad. Sci. USA, 108, 9685, 10.1073/pnas.1100062108 Arenz, 2017, The temporal tuning of the Drosophila motion detectors is determined by the dynamics of their input elements, Curr. Biol., 27, 929, 10.1016/j.cub.2017.01.051 Strother, 2014, Direct observation of ON and OFF pathways in the Drosophila visual system, Curr. Biol., 24, 976, 10.1016/j.cub.2014.03.017 Behnia, 2014, Processing properties of ON and OFF pathways for Drosophila motion detection, Nature, 512, 427, 10.1038/nature13427 Freifeld, 2013, GABAergic lateral interactions tune the early stages of visual processing in Drosophila, Neuron, 78, 1075, 10.1016/j.neuron.2013.04.024 Takemura, 2017, The comprehensive connectome of a neural substrate for ‘ON’ motion detection in Drosophila, eLife, 6, e24394, 10.7554/eLife.24394 Takemura, 2013, A visual motion detection circuit suggested by Drosophila connectomics, Nature, 500, 175, 10.1038/nature12450 Strother, 2017, The emergence of directional selectivity in the visual motion pathway of Drosophila, Neuron, 94, 168, 10.1016/j.neuron.2017.03.010 Wienecke, 2018, Linear summation underlies direction selectivity in Drosophila, Neuron, 99, 680, 10.1016/j.neuron.2018.07.005 Salazar-Gatzimas, 2016, Direct measurement of correlation responses in Drosophila elementary motion detectors reveals fast timescale tuning, Neuron, 92, 227, 10.1016/j.neuron.2016.09.017 Gruntman, 2018, Simple integration of fast excitation and offset, delayed inhibition computes directional selectivity in Drosophila, Nat. Neurosci., 21, 250, 10.1038/s41593-017-0046-4 Schnell, 2012, Columnar cells necessary for motion responses of wide-field visual interneurons in Drosophila, J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol., 198, 389, 10.1007/s00359-012-0716-3 Schilling, 2015, Local motion detectors are required for the computation of expansion flow-fields, Biol. Open, 4, 1105, 10.1242/bio.012690 Kitamoto, 2001, Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons, J. Neurobiol., 47, 81, 10.1002/neu.1018 Chen, 2013, Ultrasensitive fluorescent proteins for imaging neuronal activity, Nature, 499, 295, 10.1038/nature12354 Mauss, 2015, Neural circuit to integrate opposing motions in the visual field, Cell, 162, 351, 10.1016/j.cell.2015.06.035 Shinomiya, 2014, Candidate neural substrates for off-edge motion detection in Drosophila, Curr. Biol., 24, 1062, 10.1016/j.cub.2014.03.051 Serbe, 2016, Comprehensive characterization of the major presynaptic elements to the Drosophila OFF motion detector, Neuron, 89, 829, 10.1016/j.neuron.2016.01.006 Marvin, 2013, An optimized fluorescent probe for visualizing glutamate neurotransmission, Nat. Methods, 10, 162, 10.1038/nmeth.2333 van Hateren, 1998, Independent component filters of natural images compared with simple cells in primary visual cortex, Proc. Biol. Sci., 265, 359, 10.1098/rspb.1998.0303 Poggio, 1973, Considerations on models of movement detection, Kybernetik, 13, 223, 10.1007/BF00274887 Clark, 2014, Flies and humans share a motion estimation strategy that exploits natural scene statistics, Nat. Neurosci., 17, 296, 10.1038/nn.3600 Leonhardt, 2016, Asymmetry of Drosophila ON and OFF motion detectors enhances real-world velocity estimation, Nat. Neurosci., 19, 706, 10.1038/nn.4262 Klapoetke, 2017, Ultra-selective looming detection from radial motion opponency, Nature, 551, 237, 10.1038/nature24626 Strother, 2018, Behavioral state modulates the ON visual motion pathway of Drosophila, Proc. Natl. Acad. Sci. USA, 115, E102, 10.1073/pnas.1703090115 Yang, 2016, Subcellular imaging of voltage and calcium signals reveals neural processing in vivo, Cell, 166, 245, 10.1016/j.cell.2016.05.031 Meyer, 2014 Katsov, 2008, Motion processing streams in Drosophila are behaviorally specialized, Neuron, 59, 322, 10.1016/j.neuron.2008.05.022 Haag, 2016, Complementary mechanisms create direction selectivity in the fly, eLife, 5, 5, 10.7554/eLife.17421 Fisher, 2015, Orientation selectivity sharpens motion detection in Drosophila, Neuron, 88, 390, 10.1016/j.neuron.2015.09.033 Ramdya, 2006, Reverse correlation of rapid calcium signals in the zebrafish optic tectum in vivo, J. Neurosci. Methods, 157, 230, 10.1016/j.jneumeth.2006.04.021 Borst, 2010, Fly motion vision, Annu. Rev. Neurosci., 33, 49, 10.1146/annurev-neuro-060909-153155 Borst, 1989, Principles of visual motion detection, Trends Neurosci., 12, 297, 10.1016/0166-2236(89)90010-6 Haag, 2017, A common directional tuning mechanism of Drosophila motion-sensing neurons in the ON and in the OFF pathway, eLife, 6, e29044, 10.7554/eLife.29044 Koch, 2004 Leonhardt, 2017, Neural mechanisms underlying sensitivity to reverse-phi motion in the fly, PLoS ONE, 12, e0189019, 10.1371/journal.pone.0189019 Lee, 1999, Learning the parts of objects by non-negative matrix factorization, Nature, 401, 788, 10.1038/44565 Plumbley, M.D. (2001). Adaptive lateral inhibition for non-negative ICA. In Proceedings of the International Conference on Independent Component Analysis and Blind Signal Separation (ICA2001). pp. 516–521. Pehlevan, C., and Chklovskii, D.B. (2014). A hebbian/anti-hebbian network derived from online non-negative matrix factorization can cluster and discover sparse features. In Signals, Systems and Computers, 2014 48th Asilomar Conference (IEEE), pp. 769–775. Pehlevan, 2017, Blind nonnegative source separation using biological neural networks, Neural Comput., 29, 2925, 10.1162/neco_a_01007 Sanes, 2010, Design principles of insect and vertebrate visual systems, Neuron, 66, 15, 10.1016/j.neuron.2010.01.018 Amthor, 1993, Inhibition in ON-OFF directionally selective ganglion cells of the rabbit retina, J. Neurophysiol., 69, 2174, 10.1152/jn.1993.69.6.2174 Grzywacz, 1993, Facilitation in ON-OFF directionally selective ganglion cells of the rabbit retina, J. Neurophysiol., 69, 2188, 10.1152/jn.1993.69.6.2188 Famiglietti, 1983, ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric on and off amacrine cells of rabbit retina, Brain Res., 261, 138, 10.1016/0006-8993(83)91293-3 Fransen, 2017, Temporally diverse excitation generates direction-selective responses in ON- and OFF-type retinal starburst amacrine cells, Cell Rep., 18, 1356, 10.1016/j.celrep.2017.01.026 Mo, 2003, Modeling reverse-phi motion-selective neurons in cortex: Double synaptic-veto mechanism, Neural Comput., 15, 735, 10.1162/08997660360581886 Chalasani, 2007, Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans, Nature, 450, 63, 10.1038/nature06292 Gallio, 2011, The coding of temperature in the Drosophila brain, Cell, 144, 614, 10.1016/j.cell.2011.01.028 Matsuo, 2014, Identification of novel vibration- and deflection-sensitive neuronal subgroups in Johnston’s organ of the fruit fly, Front. Physiol., 5, 179, 10.3389/fphys.2014.00179 Mazor, 2005, Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons, Neuron, 48, 661, 10.1016/j.neuron.2005.09.032 Scholl, 2010, Nonoverlapping sets of synapses drive on responses and off responses in auditory cortex, Neuron, 65, 412, 10.1016/j.neuron.2010.01.020 Gjorgjieva, 2014, Benefits of pathway splitting in sensory coding, J. Neurosci., 34, 12127, 10.1523/JNEUROSCI.1032-14.2014 Ratliff, 2010, Retina is structured to process an excess of darkness in natural scenes, Proc. Natl. Acad. Sci. USA, 107, 17368, 10.1073/pnas.1005846107 Simoncelli, 2001, Natural image statistics and neural representation, Annu. Rev. Neurosci., 24, 1193, 10.1146/annurev.neuro.24.1.1193 Dyakova, 2015, A higher order visual neuron tuned to the spatial amplitude spectra of natural scenes, Nat. Commun., 6, 8522, 10.1038/ncomms9522 Field, 1993, Scale-invariance and self-similar ‘wavelet’ transforms: An analysis of natural scenes and mammalian visual systems, 151 Ruderman, 1994, Statistics of natural images: Scaling in the woods, Phys. Rev. Lett., 73, 814, 10.1103/PhysRevLett.73.814 Vinje, 2000, Sparse coding and decorrelation in primary visual cortex during natural vision, Science, 287, 1273, 10.1126/science.287.5456.1273 Nitzany, 2014, The statistics of local motion signals in naturalistic movies, J. Vis., 14 Srinivasan, 1982, Predictive coding: A fresh view of inhibition in the retina, Proc. R. Soc. Lond. B Biol. Sci., 216, 427, 10.1098/rspb.1982.0085 Atick, 1990, Towards a theory of early visual processing, Neural Comput., 2, 308, 10.1162/neco.1990.2.3.308 Bell, 1997, The “independent components” of natural scenes are edge filters, Vision Res., 37, 3327, 10.1016/S0042-6989(97)00121-1 Kastner, 2015, Critical and maximally informative encoding between neural populations in the retina, Proc. Natl. Acad. Sci. USA, 112, 2533, 10.1073/pnas.1418092112 Pitkow, 2012, Decorrelation and efficient coding by retinal ganglion cells, Nat. Neurosci., 15, 628, 10.1038/nn.3064 Simmons, 2013, Transformation of stimulus correlations by the retina, PLoS Comput. Biol., 9, e1003344, 10.1371/journal.pcbi.1003344 Westheimer, 2007, The ON-OFF dichotomy in visual processing: From receptors to perception, Prog. Retin. Eye Res., 26, 636, 10.1016/j.preteyeres.2007.07.003 Fiete, 2004, Temporal sparseness of the premotor drive is important for rapid learning in a neural network model of birdsong, J. Neurophysiol., 92, 2274, 10.1152/jn.01133.2003 Nordström, 2006, Insect detection of small targets moving in visual clutter, PLoS Biol., 4, e54, 10.1371/journal.pbio.0040054 Keleş, 2017, Object-detecting neurons in Drosophila, Curr. Biol., 27, 680, 10.1016/j.cub.2017.01.012 Stork, 2014, Neuron-glia interactions through the Heartless FGF receptor signaling pathway mediate morphogenesis of Drosophila astrocytes, Neuron, 83, 388, 10.1016/j.neuron.2014.06.026 Gohl, 2011, A versatile in vivo system for directed dissection of gene expression patterns, Nat. Methods, 8, 231, 10.1038/nmeth.1561 Brainard, 1997, The psychophysics toolbox, Spat. Vis., 10, 433, 10.1163/156856897X00357 Pologruto, 2003, ScanImage: Flexible software for operating laser scanning microscopes, Biomed. Eng. Online, 2, 13, 10.1186/1475-925X-2-13 Wilson, 2004, Transformation of olfactory representations in the Drosophila antennal lobe, Science, 303, 366, 10.1126/science.1090782 Mano, 2017, Graphics processing unit-accelerated code for computing second-order wiener kernels and spike-triggered covariance, PLoS ONE, 12, e0169842, 10.1371/journal.pone.0169842