Rapid categorization of achromatic natural scenes: how robust at very low contrasts?

The human visual system is remarkably good at categorizing objects even in challenging visual conditions. Here we specifically assessed the robustness of the visual system in the face of large contrast variations in a high‐level categorization task using natural images. Human subjects performed a go/no‐go animal/nonanimal categorization task with briefly flashed grey level images. Performance was analysed for a large range of contrast conditions randomly presented to the subjects and varying from normal to 3% of initial contrast. Accuracy was very robust and subjects were performing well above chance level (≈ 70% correct) with only 10–12% of initial contrast. Accuracy decreased with contrast reduction but reached chance level only in the most extreme condition (3% of initial contrast). Conversely, the maximal increase in mean reaction time was ≈ 60 ms (at 8% of initial contrast); it then remained stable with further contrast reductions. Associated ERPs recorded on correct target and distractor trials showed a clear differential effect whose amplitude and peak latency were correlated respectively with task accuracy and mean reaction times. These data show the strong robustness of the visual system in object categorization at very low contrast. They suggest that magnocellular information could play a role in ventral stream visual functions such as object recognition. Performance may rely on early object representations which lack the details provided subsequently by the parvocellular system but contain enough information to reach decision in the categorization task.

[1]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[2]  R. L. de Valois,et al.  Psychophysical studies of monkey vision. 3. Spatial luminance contrast sensitivity tests of macaque and human observers. , 1974, Vision research.

[3]  W. Wolf,et al.  Perceptual latencies to sinusoidal gratings , 1976, Vision Research.

[4]  M. Potter Short-term conceptual memory for pictures. , 1976, Journal of experimental psychology. Human learning and memory.

[5]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[6]  R. Shapley,et al.  Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque , 1981, Nature.

[7]  D. G. Albrecht,et al.  Striate cortex of monkey and cat: contrast response function. , 1982, Journal of neurophysiology.

[8]  D. F. Fisher,et al.  Eye movements : cognition and visual perception , 1982 .

[9]  R. Shapley,et al.  X and Y cells in the lateral geniculate nucleus of macaque monkeys. , 1982, The Journal of physiology.

[10]  G. Blasdel,et al.  Physiological organization of layer 4 in macaque striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[12]  S. Sherman Functional organization of the W-, X-, and Y- cell pathways in the cat: A review and hypothesis , 1985 .

[13]  William H. Merigan,et al.  Spatio-temporal vision of macaques with severe loss of Pβ retinal ganglion cells , 1986, Vision Research.

[14]  R. Shapley,et al.  The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Sestokas,et al.  Visual response latency of X- and Y-cells in the dorsal lateral geniculate nucleus of the cat , 1986, Vision Research.

[16]  K. Kratz,et al.  Visual latency of ganglion X- and Y-cells: A comparison with geniculate X- and Y-cells , 1987, Vision Research.

[17]  E Kaplan,et al.  Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. , 1987, The Journal of physiology.

[18]  Gordon E. Legge,et al.  Psychophysics of reading—V. The role of contrast in normal vision , 1987, Vision Research.

[19]  Barry B. Lee,et al.  Chapter 7 New views of primate retinal function , 1990 .

[20]  DH Hubel,et al.  Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  N. Logothetis,et al.  Role of the color-opponent and broad-band channels in vision , 1990, Visual Neuroscience.

[22]  P. Lennie,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[23]  R Shapley,et al.  Visual sensitivity and parallel retinocortical channels. , 1990, Annual review of psychology.

[24]  V. Perry,et al.  The topography of magnocellular projecting ganglion cells (M-ganglion cells) in the primate retina , 1991, Neuroscience.

[25]  I. Rentschler,et al.  Contrast thresholds for identification of numeric characters in direct and eccentric view , 1991, Perception & psychophysics.

[26]  P Heggelund,et al.  The effect of contrast on the visual response of lagged and nonlagged cells in the cat lateral geniculate nucleus. , 1992, Visual neuroscience.

[27]  A B Watson,et al.  Transfer of contrast sensitivity in linear visual networks , 1992, Visual Neuroscience.

[28]  J. Maunsell,et al.  Visual response latencies in striate cortex of the macaque monkey. , 1992, Journal of neurophysiology.

[29]  D. Dacey,et al.  Dendritic field size and morphology of midget and parasol ganglion cells of the human retina. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[30]  D. Dacey,et al.  A coupled network for parasol but not midget ganglion cells in the primate retina , 1992, Visual Neuroscience.

[31]  J. Maunsell,et al.  Mixed parvocellular and magnocellular geniculate signals in visual area V4 , 1992, Nature.

[32]  Leslie G. Ungerleider,et al.  The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  D. Ruderman The statistics of natural images , 1994 .

[34]  J. Maunsell,et al.  Magnocellular and parvocellular contributions to the responses of neurons in macaque striate cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  E. Halgren,et al.  Spatio-temporal stages in face and word processing. 2. Depth-recorded potentials in the human frontal and Rolandic cortices , 1994, Journal of Physiology-Paris.

[36]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[37]  J. Bullier,et al.  Visual latencies in areas V1 and V2 of the macaque monkey , 1995, Visual Neuroscience.

[38]  Michael D. Rugg,et al.  Word and Nonword Repetition Within- and Across-Modality: An Event-Related Potential Study , 1995, Journal of Cognitive Neuroscience.

[39]  D. G. Albrecht Visual cortex neurons in monkey and cat: Effect of contrast on the spatial and temporal phase transfer functions , 1995, Visual Neuroscience.

[40]  H Strasburger,et al.  Contrast‐dependent Dissociation of Visual Recognition and Detection Fields , 1996, The European journal of neuroscience.

[41]  B. Richmond,et al.  Latency: another potential code for feature binding in striate cortex. , 1996, Journal of neurophysiology.

[42]  Denis Fize,et al.  Speed of processing in the human visual system , 1996, Nature.

[43]  S. Thorpe,et al.  Rapid categorization of natural images by rhesus monkeys , 1998, Neuroreport.

[44]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[45]  Kenji Kawano,et al.  Global and fine information coded by single neurons in the temporal visual cortex , 1999, Nature.

[46]  Trichur Raman Vidyasagar A neuronal model of attentional spotlight: parietal guiding the temporal , 1999, Brain Research Reviews.

[47]  J. Maunsell,et al.  Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys , 1999, Visual Neuroscience.

[48]  D J Field,et al.  Local Contrast in Natural Images: Normalisation and Coding Efficiency , 2000, Perception.

[49]  J. Rieger,et al.  Sensory and cognitive contributions of color to the recognition of natural scenes , 2000, Current Biology.

[50]  G Richard,et al.  Ultra-rapid categorisation of natural scenes does not rely on colour cues: a study in monkeys and humans , 2000, Vision Research.

[51]  G. Kovács,et al.  Early and late components of visual categorization: an event-related potential study. , 2000, Brain research. Cognitive brain research.

[52]  D. Tolhurst,et al.  Calculating the contrasts that retinal ganglion cells and LGN neurones encounter in natural scenes , 2000, Vision Research.

[53]  Ilpo Kojo,et al.  Effect of stimulus contrast on performance and eye movements in visual search , 2001, Vision Research.

[54]  F. Mechler,et al.  Temporal coding of contrast in primary visual cortex: when, what, and why. , 2001, Journal of neurophysiology.

[55]  G. V. Simpson,et al.  Flow of activation from V1 to frontal cortex in humans , 2001, Experimental Brain Research.

[56]  J. Pokorny,et al.  Rod-cone interactions assessed in inferred magnocellular and parvocellular postreceptoral pathways. , 2001, Journal of vision.

[57]  Gordon E Legge,et al.  Psychophysics of reading XX. Linking letter recognition to reading speed in central and peripheral vision , 2001, Vision Research.

[58]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[59]  R VanRullen,et al.  Is it a Bird? Is it a Plane? Ultra-Rapid Visual Categorisation of Natural and Artifactual Objects , 2001, Perception.

[60]  P. Fldik,et al.  The Speed of Sight , 2001, Journal of Cognitive Neuroscience.

[61]  Jeffrey D. Schall,et al.  Neural basis of deciding, choosing and acting , 2001, Nature Reviews Neuroscience.

[62]  S. Thorpe,et al.  The Time Course of Visual Processing: From Early Perception to Decision-Making , 2001, Journal of Cognitive Neuroscience.

[63]  J. Kulikowski,et al.  Convergence of parvocellular and magnocellular information channels in the primary visual cortex of the macaque , 2002, The European journal of neuroscience.

[64]  Robert A. Frazor,et al.  Visual cortex neurons of monkeys and cats: temporal dynamics of the contrast response function. , 2002, Journal of neurophysiology.

[65]  M W Oram,et al.  The temporal resolution of neural codes: does response latency have a unique role? , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[66]  A. Proverbio,et al.  Early involvement of the temporal area in attentional selection of grating orientation: an ERP study. , 2002, Brain research. Cognitive brain research.

[67]  N. Kanwisher,et al.  Stages of processing in face perception: an MEG study , 2002, Nature Neuroscience.

[68]  S. Thorpe,et al.  Surfing a spike wave down the ventral stream , 2002, Vision Research.

[69]  Guillaume A. Rousselet,et al.  Parallel processing in high-level categorization of natural images , 2002, Nature Neuroscience.

[70]  T. Hendler,et al.  Contrast sensitivity in human visual areas and its relationship to object recognition. , 2002, Journal of neurophysiology.

[71]  Bruno A Olshausen,et al.  Timecourse of neural signatures of object recognition. , 2003, Journal of vision.

[72]  Michael B. Lewis,et al.  Face Detection: Mapping Human Performance , 2003, Perception.

[73]  Michèle Fabre-Thorpe,et al.  Interaction of top-down and bottom-up processing in the fast visual analysis of natural scenes. , 2004, Brain research. Cognitive brain research.

[74]  G. Berlucchi,et al.  Lesion of areas 17/18/19: effects on the cat's performance in a binary detection task , 2004, Experimental Brain Research.

[75]  Trichur R Vidyasagar,et al.  The role of the magnocellular pathway in serial deployment of visual attention , 2004, The European journal of neuroscience.

[76]  E. Rolls,et al.  Size and contrast have only small effects on the responses to faces of neurons in the cortex of the superior temporal sulcus of the monkey , 2004, Experimental Brain Research.

[77]  Guillaume A. Rousselet,et al.  Processing of one, two or four natural scenes in humans: the limits of parallelism , 2004, Vision Research.

[78]  S. Thorpe,et al.  The time course of visual processing: Backward masking and natural scene categorisation , 2005, Vision Research.