Invisible noise obscures visible signal in insect motion detection

The motion energy model is the standard account of motion detection in animals from beetles to humans. Despite this common basis, we show here that a difference in the early stages of visual processing between mammals and insects leads this model to make radically different behavioural predictions. In insects, early filtering is spatially lowpass, which makes the surprising prediction that motion detection can be impaired by “invisible” noise, i.e. noise at a spatial frequency that elicits no response when presented on its own as a signal. We confirm this prediction using the optomotor response of praying mantis Sphodromantis lineola. This does not occur in mammals, where spatially bandpass early filtering means that linear systems techniques, such as deriving channel sensitivity from masking functions, remain approximately valid. Counter-intuitive effects such as masking by invisible noise may occur in neural circuits wherever a nonlinearity is followed by a difference operation.

[1]  E. Buchner Elementary movement detectors in an insect visual system , 1976, Biological Cybernetics.

[2]  J. van Santen,et al.  Temporal covariance model of human motion perception. , 1984, Journal of the Optical Society of America. A, Optics and image science.

[3]  C Blakemore,et al.  On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images , 1969, The Journal of physiology.

[4]  D. Burr Sensitivity to spatial phase , 1980, Vision Research.

[5]  R. Sekuler,et al.  The independence of channels in human vision selective for direction of movement. , 1975, The Journal of physiology.

[6]  E J Chichilnisky,et al.  A simple white noise analysis of neuronal light responses , 2001, Network.

[7]  D. Pollen,et al.  Cross-correlation analyses of nonlinear systems with spatiotemporal inputs (visual neurons) , 1993, IEEE Transactions on Biomedical Engineering.

[8]  S. Laughlin,et al.  Spatio-temporal properties of motion detectors matched to low image velocities in hovering insects , 1997, Vision Research.

[9]  J. Robson Spatial and Temporal Contrast-Sensitivity Functions of the Visual System , 1966 .

[10]  Eero P. Simoncelli,et al.  Spatiotemporal Elements of Macaque V1 Receptive Fields , 2005, Neuron.

[11]  E. Adelson,et al.  Directionally selective complex cells and the computation of motion energy in cat visual cortex , 1992, Vision Research.

[12]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[13]  Nicole C. Rust,et al.  Do We Know What the Early Visual System Does? , 2005, The Journal of Neuroscience.

[14]  J. Movshon,et al.  Spatial summation in the receptive fields of simple cells in the cat's striate cortex. , 1978, The Journal of physiology.

[15]  Matteo Carandini,et al.  What simple and complex cells compute , 2006, The Journal of physiology.

[16]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[17]  D. Badcock Spatial phase or luminance profile discrimination? , 1984, Vision Research.

[18]  Samuel Rossel,et al.  Regional differences in photoreceptor performance in the eye of the praying mantis , 1979, Journal of comparative physiology.

[19]  K. D. De Valois,et al.  Spatial‐frequency‐specific inhibition in cat striate cortex cells. , 1983, The Journal of physiology.

[20]  L. O. Harvey,et al.  Visual texture perception and Fourier analysis , 1978, Perception & psychophysics.

[21]  B. Julesz,et al.  Spatial-frequency masking in vision: critical bands and spread of masking. , 1972, Journal of the Optical Society of America.

[22]  D Marr,et al.  Theory of edge detection , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[23]  M. J. Morgan,et al.  Spatial filtering precedes motion detection , 1992, Nature.

[24]  A. Borst,et al.  Common circuit design in fly and mammalian motion vision , 2015, Nature Neuroscience.

[25]  Michael J. Berry,et al.  The Neural Code of the Retina , 1999, Neuron.

[26]  G. J. Burton,et al.  Evidence for non-linear response processes in the human visual system from measurements on the thresholds of spatial beat frequencies. , 1973, Vision research.

[27]  C. W. G Clifford,et al.  Fundamental mechanisms of visual motion detection: models, cells and functions , 2002, Progress in Neurobiology.

[28]  David C. Burr,et al.  Smooth and sampled motion , 1986, Vision Research.

[29]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[30]  C L Baker,et al.  A processing stream in mammalian visual cortex neurons for non-Fourier responses. , 1993, Science.

[31]  L. Maffei,et al.  The visual cortex as a spatial frequency analyser. , 1973, Vision research.

[32]  D. Burr,et al.  Seeing objects in motion , 1986, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[33]  N. Graham,et al.  Detection of grating patterns containing two spatial frequencies: a comparison of single-channel and multiple-channels models. , 1971, Vision research.

[34]  R A Andersen,et al.  Transparent motion perception as detection of unbalanced motion signals. III. Modeling , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Jenny C. A. Read,et al.  The contrast sensitivity function of the praying mantis Sphodromantis lineola , 2015, Journal of Comparative Physiology A.

[36]  D. Pollen,et al.  Responses of simple and complex cells to compound sine-wave gratings , 1988, Vision Research.

[37]  J. Daugman Spatial visual channels in the fourier plane , 1984, Vision Research.

[38]  G. Legge Adaptation to a spatial impulse: Implications for Fourier transform models of visual processing , 1976, Vision Research.

[39]  D. Burr,et al.  Spatial and temporal selectivity of the human motion detection system , 1985, Vision Research.

[40]  B. Hassenstein,et al.  Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus , 1956 .

[41]  J. van Santen,et al.  Elaborated Reichardt detectors. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[42]  D. Burr,et al.  Feature detection in human vision: a phase-dependent energy model , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[43]  G. Sperling,et al.  The functional architecture of human visual motion perception , 1995, Vision Research.

[44]  S. Laughlin,et al.  Insect motion detectors matched to visual ecology , 1996, Nature.

[45]  Allan W. Snyder,et al.  Spatial information capacity of compound eyes , 2004, Journal of comparative physiology.

[46]  J. Movshon,et al.  Receptive field organization of complex cells in the cat's striate cortex. , 1978, The Journal of physiology.

[47]  R. Patterson,et al.  Off-frequency listening and auditory-filter asymmetry. , 1980, The Journal of the Acoustical Society of America.

[48]  Helder Araújo,et al.  Stereoscopic Depth Perception Using a Model Based on the Primary Visual Cortex , 2013, PloS one.

[49]  Mandyam V. Srinivasan,et al.  The contrast sensitivity of fly movement-detecting neurons , 1980, Vision Research.

[50]  Erich Buchner,et al.  Visual movement detection under light- and dark-adaptation in the fly,Musca domestica , 1979, Journal of comparative physiology.

[51]  M. J. Korenberg,et al.  The identification of nonlinear biological systems: Wiener and Hammerstein cascade models , 1986, Biological Cybernetics.

[52]  T. B. Lawton,et al.  The effect of phase structures on spatial phase discrimination , 1984, Vision Research.

[53]  W. Geisler,et al.  Optimal disparity estimation in natural stereo images. , 2014, Journal of vision.

[54]  A. Borst Neural Circuits for Elementary Motion Detection , 2014, Journal of neurogenetics.

[55]  J. Robson,et al.  Application of fourier analysis to the visibility of gratings , 1968, The Journal of physiology.

[56]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[57]  David C. Burr,et al.  Receptive field properties of human motion detector units inferred from spatial frequency masking , 1989, Vision Research.

[58]  Ignacio Serrano-Pedraza,et al.  The optomotor response of the praying mantis is driven predominantly by the central visual field , 2016, Journal of Comparative Physiology A.

[59]  J. Robson,et al.  Spatial-frequency channels in human vision. , 1971, Journal of the Optical Society of America.