Learning to be fast: Gain accuracy with speed

Our recent neurophysiological findings provided evidence for collinear facilitation in detecting low-contrast Gabor patches (GPs) and for the abolishment of these collinear interactions by backward masking (BM) (Sterkin et al., 2008; Sterkin, Yehezkel, Bonneh, et al., 2009). We suggested that the suppression induced by the BM eliminates the collinear facilitation. Moreover, our recent study showed that training on a BM task overcomes the BM effect, hence, improves the processing speed (Polat, 2009). Here we applied training on detecting a target that is followed by BM in order to study whether reinforced facilitatory interactions can overcome the suppressive effects induced by BM. Event-Related Potentials (ERPs) were recorded before and after ten training sessions performed on different days. Low-contrast, foveal target GP was simultaneously flanked by two collinear high-contrast GPs. In the BM task, another identical mask was presented at different time-intervals (ISIs). Before training, BM induced suppression of target detection, at the ISI of 50 ms, in agreement with earlier behavioral findings. This ISI coincides with the active time-window of lateral interactions. After training, our results show a remarkable improvement in all behavioral measurements, including percent of correct responses, sensitivity (d'), reaction time (RT) and the decision criterion for this ISI. The ERP results show that before training,BM attenuated the physiological markers of facilitation at the same ISI of 50 ms, measured as the amplitude of the negative N1 peak (latency of 260 ms). After the training, the sensory representation, reflected by P1 peak, has not changed, consistent with the unchanged physical parameters of the stimulus. Instead, the shorter latency (by 20 ms, latency of 240 ms) and the increased amplitude of N1 represent the development of faster and stronger facilitatory lateral interactions between the target and the collinear flankers. Thus, previously effective backward masking became ineffective in disrupting the collinear facilitation. Moreover, a high-amplitude late peak (P4, latency of 610-630 ms) was not affected by training, however its high correlation with RT (95%) before training was significantly decreased (to 76%), consistent with a lower-level representation of a trained skill. We suggest that perceptual learning that strengthens collinear facilitation results in a faster processing speed.

[1]  U. Polat,et al.  Contrast response characteristics of long-range lateral interactions in cat striate cortex , 2001, Neuroreport.

[2]  Y. Frégnac,et al.  Visual input evokes transient and strong shunting inhibition in visual cortical neurons , 1998, Nature.

[3]  D. Sagi,et al.  Isolating Excitatory and Inhibitory Nonlinear Spatial Interactions Involved in Contrast Detection * * Part of this paper was presented at the 17th ECVP conference, Eindhoven, The Netherlands (September 1994). , 1996, Vision Research.

[4]  G. Rees,et al.  Fine-scale activity patterns in high-level visual areas encode the category of invisible objects. , 2008, Journal of vision.

[5]  D. Scott Perceptual learning. , 1974, Queen's nursing journal.

[6]  U. Polat,et al.  Major Depression Affects Perceptual Filling-In , 2008, Biological Psychiatry.

[7]  W Singer,et al.  The Perceptual Grouping Criterion of Colinearity is Reflected by Anisotropies of Connections in the Primary Visual Cortex , 1997, The European journal of neuroscience.

[8]  D. Sagi,et al.  Long-lasting, long-range detection facilitation , 1998, Vision Research.

[9]  Oov Sagl Plasticity of Spatial Interactions in Early Vision , 1995 .

[10]  U. Polat,et al.  The architecture of perceptual spatial interactions , 1994, Vision Research.

[11]  C. Gilbert,et al.  Learning to see: experience and attention in primary visual cortex , 2001, Nature Neuroscience.

[12]  T. Wiesel,et al.  Intrinsic connectivity and receptive field properties in visual cortex , 1985, Vision Research.

[13]  D. Sagi,et al.  Psychometric curves of lateral facilitation. , 2006, Spatial vision.

[14]  G. R. Mangun,et al.  Electrophysiological correlates of lateral interactions in human visual cortex , 2004, Vision Research.

[15]  D. Sagi,et al.  Top-Down Modulation of Lateral Interactions in Early Vision Does Attention Affect Integration of the Whole or Just Perception of the Parts? , 2003, Current Biology.

[16]  D. Sagi Perceptual learning in Vision Research , 2011, Vision Research.

[17]  C D Gilbert,et al.  Early perceptual learning. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Takeo Watanabe,et al.  Advances in visual perceptual learning and plasticity , 2010, Nature Reviews Neuroscience.

[19]  Chang-Bing Huang,et al.  Perceptual Learning Improves Contrast Sensitivity of V1 Neurons in Cats , 2010, Current Biology.

[20]  Y. Frégnac,et al.  The “silent” surround of V1 receptive fields: theory and experiments , 2003, Journal of Physiology-Paris.

[21]  R. Frostig,et al.  Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  U. Polat,et al.  Collinear stimuli regulate visual responses depending on cell's contrast threshold , 1998, Nature.

[23]  Zoe Kourtzi,et al.  Flexible learning of natural statistics in the human brain. , 2009, Journal of neurophysiology.

[24]  J. Movshon,et al.  Time Course and Time-Distance Relationships for Surround Suppression in Macaque V1 Neurons , 2003, The Journal of Neuroscience.

[25]  Uri Polat,et al.  Restoration of underdeveloped cortical functions: evidence from treatment of adult amblyopia. , 2008, Restorative neurology and neuroscience.

[26]  D. Tanné,et al.  Perceptual learning: learning to see , 1994, Current Opinion in Neurobiology.

[27]  C. Gilbert,et al.  Attention Modulates Contextual Influences in the Primary Visual Cortex of Alert Monkeys , 1999, Neuron.

[28]  D. Sagi,et al.  Excitatory-inhibitory network in the visual cortex: psychophysical evidence. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[29]  K. Svoboda,et al.  Experience-dependent structural synaptic plasticity in the mammalian brain , 2009, Nature Reviews Neuroscience.

[30]  S. Hochstein,et al.  View from the Top Hierarchies and Reverse Hierarchies in the Visual System , 2002, Neuron.

[31]  A. Angelucci,et al.  Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. , 2006, Progress in brain research.

[32]  C. Gilbert,et al.  The Neural Basis of Perceptual Learning , 2001, Neuron.

[33]  Charles D. Gilbert,et al.  The Role of Horizontal Connections in Generating Long Receptive Fields in the Cat Visual Cortex , 1989, The European journal of neuroscience.

[34]  C. Gilbert,et al.  Learning to Link Visual Contours , 2008, Neuron.

[35]  Takeo Watanabe,et al.  Accounting for speed–accuracy tradeoff in perceptual learning , 2012, Vision Research.

[36]  Z Liu,et al.  Simultaneous learning of motion discrimination in two directions. , 1998, Brain research. Cognitive brain research.

[37]  U. Polat,et al.  Neurophysiological Evidence for Contrast Dependent Long-range Facilitation and Suppression in the Human Visual Cortex , 1996, Vision Research.

[38]  T. Wiesel,et al.  Functional organization of the visual cortex. , 1983, Progress in brain research.

[39]  U. Polat,et al.  What pattern the eye sees best , 1999, Vision Research.

[40]  D Sagi,et al.  Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[41]  T. Kasamatsu,et al.  Collinear facilitation is independent of receptive-field expansion at low contrast , 2009, Experimental Brain Research.

[42]  Gianluca Campana,et al.  Perceptual learning modulates electrophysiological and psychophysical response to visual texture segmentation in humans , 2004, Neuroscience Letters.

[43]  H. Spitzer,et al.  Chromatic collinear facilitation, further evidence for chromatic form perception. , 2006, Spatial vision.

[44]  Dov Sagi,et al.  Early-vision brain responses which predict human visual segmentation and learning. , 2009, Journal of vision.

[45]  Siegrid Löwel,et al.  GABA-inactivation attenuates colinear facilitation in cat primary visual cortex , 2002, Experimental Brain Research.

[46]  Uri Polat,et al.  Backward masking suppresses collinear facilitation in the visual cortex , 2009, Vision Research.

[47]  Paul T. Sowden,et al.  Perceptual learning of luminance contrast detection: specific for spatial frequency and retinal location but not orientation , 2002, Vision Research.

[48]  U. Polat,et al.  Lateral interactions between spatial channels: Suppression and facilitation revealed by lateral masking experiments , 1993, Vision Research.

[49]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  E. Peli,et al.  Lateral interactions: size does matter , 2002, Vision Research.

[51]  G. Pourtois,et al.  Effects of perceptual learning on primary visual cortex activity in humans , 2008, Vision Research.

[52]  R. Hess,et al.  The dynamics of collinear facilitation: Fast but sustained , 2008, Vision Research.

[53]  M. Fahle Perceptual learning: specificity versus generalization , 2005, Current Opinion in Neurobiology.

[54]  A. Fiorentini,et al.  Perceptual learning specific for orientation and spatial frequency , 1980, Nature.

[55]  U Polat,et al.  Facilitation and suppression of single striate-cell activity by spatially discrete pattern stimuli presented beyond the receptive field , 2001, Visual Neuroscience.

[56]  Branka Spehar,et al.  Dynamics of collinear contrast facilitation are consistent with long-range horizontal striate transmission , 2005, Vision Research.

[57]  S. Klein,et al.  Suppressive and facilitatory spatial interactions in amblyopic vision , 2002, Vision Research.

[58]  C W Tyler,et al.  Spatial pattern summation is phase-insensitive in the fovea but not in the periphery. , 1999, Spatial vision.

[59]  Uri Polat,et al.  Making perceptual learning practical to improve visual functions , 2009, Vision Research.

[60]  Leslie G. Ungerleider,et al.  The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Takeo Watanabe,et al.  Accounting for speed-accuracy tradeoff in visual perceptual learning , 2010 .

[62]  Jon Driver,et al.  Lateral interactions between targets and flankers in low-level vision depend on attention to the flankers , 2001, Nature Neuroscience.

[63]  David Alais,et al.  The mechanisms of collinear integration. , 2006, Journal of vision.

[64]  U. Polat,et al.  Response similarity as a basis for perceptual binding. , 2008, Journal of vision.

[65]  Roger Ratcliff,et al.  Dissociable Perceptual-learning Mechanisms Revealed by Diffusion-model Analysis , 2022 .

[66]  Michael H. Herzog,et al.  Perceptual learning and roving: Stimulus types and overlapping neural populations , 2009, Vision Research.

[67]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[68]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[69]  Michael H. Herzog,et al.  Effects of grouping in contextual modulation , 2002, Nature.

[70]  U Polat,et al.  Spatial interactions in human vision: from near to far via experience-dependent cascades of connections. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[71]  C. Gilbert,et al.  Perceptual learning and adult cortical plasticity , 2009, The Journal of physiology.

[72]  D. Fitzpatrick The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. , 1996, Cerebral cortex.

[73]  Pengjing Xu,et al.  Perceptual learning improves contrast sensitivity and visual acuity in adults with anisometropic amblyopia , 2006, Vision Research.

[74]  U. Polat Functional architecture of long-range perceptual interactions. , 1999, Spatial vision.

[75]  D. Sagi,et al.  Configuration saliency revealed in short duration binocular rivalry , 1999, Vision Research.

[76]  M. Morgan,et al.  Facilitation from collinear flanks is cancelled by non-collinear flanks , 2000, Vision Research.

[77]  S. Maier,et al.  Widespread Periodic Intrinsic Connections in the Tree Shrew Visual Cortex , 2005 .

[78]  Manfred Fahle,et al.  Perceptual learning: gain without pain? , 2002, Nature Neuroscience.

[79]  Uri Polat,et al.  Spatio-temporal low-level neural networks account for visual masking , 2008, Advances in cognitive psychology.

[80]  Vision Research , 1961, Nature.

[81]  Uri Polat,et al.  The relationship between the subjective and objective aspects of visual filling-in , 2007, Vision Research.

[82]  Hamutal Slovin,et al.  Population response to contextual influences in the primary visual cortex. , 2010, Cerebral cortex.

[83]  Michael Belkin,et al.  Improving vision in adult amblyopia by perceptual learning. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[84]  C. Gilbert,et al.  Improvement in visual sensitivity by changes in local context: Parallel studies in human observers and in V1 of alert monkeys , 1995, Neuron.

[85]  Uri Polat,et al.  Multi-component correlate for lateral collinear interactions in the human visual cortex , 2008, Vision Research.

[86]  H. B. Barlow,et al.  What does the eye see best? , 1983, Nature.

[87]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[88]  D. Sagi,et al.  Recurrent networks in human visual cortex: psychophysical evidence. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

[89]  Eli Peli,et al.  Facilitation of contrast detection in near-peripheral vision , 2004, Vision Research.