Rewards Evoke Learning of Unconsciously Processed Visual Stimuli in Adult Humans

The study of human learning is complicated by the myriad of processing elements involved in conducting any behavioral task. In the case of visual perceptual learning, there has been significant controversy regarding the task processes that guide the formation of this learning. However, there is a developing consensus that top-down, task-related factors are required for such learning to take place. Here we challenge this idea by use of a novel procedure in which human participants, who were deprived of food and water, passively viewed visual stimuli while receiving occasional drops of water as rewards. Visual orientation stimuli, which were temporally paired with the liquid rewards, were viewed monocularly and rendered imperceptible by continuously flashing contour-rich patterns to the other eye. Results show that visual learning can be formed in human adults through stimulus-reward pairing in the absence of a task and without awareness of the stimulus presentation or reward contingencies.

[1]  Pierre Jolicoeur,et al.  Requirement for high-level processing in subliminal learning , 2005, Current Biology.

[2]  José E. Náñez,et al.  Greater plasticity in lower-level than higher-level visual motion processing in a passive perceptual learning task , 2002, Nature Neuroscience.

[3]  P. Glimcher,et al.  Activity in Posterior Parietal Cortex Is Correlated with the Relative Subjective Desirability of Action , 2004, Neuron.

[4]  Aaron R. Seitz,et al.  Psychophysics: Is subliminal learning really passive? , 2003, Nature.

[5]  Takeo Watanabe,et al.  Perceptual learning without perception , 2001, Nature.

[6]  Karl J. Friston,et al.  Cholinergic Modulation of Experience-Dependent Plasticity in Human Auditory Cortex , 2002, Neuron.

[7]  Mitsuo Kawato,et al.  Effect of spatial distance to the task stimulus on task-irrelevant perceptual learning of static Gabors. , 2007, Journal of vision.

[8]  Michael M Merzenich,et al.  Perceptual Learning Directs Auditory Cortical Map Reorganization through Top-Down Influences , 2006, The Journal of Neuroscience.

[9]  S. Hochstein,et al.  Attentional control of early perceptual learning. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[10]  W. Schultz.  Multiple reward signals in the brain , 2000, Nature Reviews Neuroscience.

[11]  Steven R. Holloway,et al.  Visual experience can substantially alter critical flicker fusion thresholds , 2005, Human psychopharmacology.

[12]  Angela J. Yu,et al.  Uncertainty, Neuromodulation, and Attention , 2005, Neuron.

[13]  R. von der Heydt,et al.  Illusory contours and cortical neuron responses. , 1984, Science.

[14]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[15]  S. Nishida,et al.  Complete interocular transfer of motion aftereffect with flickering test , 1994, Vision Research.

[16]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[17]  C. Gilbert,et al.  Perceptual learning and top-down influences in primary visual cortex , 2004, Nature Neuroscience.

[18]  C. Koch,et al.  Continuous flash suppression reduces negative afterimages , 2005, Nature Neuroscience.

[19]  Aaron R. Seitz,et al.  A common framework for perceptual learning , 2007, Current Opinion in Neurobiology.

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

[21]  Bruce D. McCandliss,et al.  Testing the Efficiency and Independence of Attentional Networks , 2002, Journal of Cognitive Neuroscience.

[22]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[23]  S. Hochstein,et al.  Task difficulty and the specificity of perceptual learning , 1997, Nature.

[24]  N. Logothetis,et al.  Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry , 1996, Nature.

[25]  H. Pashler,et al.  Improvement in line orientation discrimination is retinally local but dependent on cognitive set , 1992, Perception & psychophysics.

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

[27]  B. Dosher,et al.  Perceptual learning without feedback in non-stationary contexts: Data and model , 2006, Vision Research.

[28]  M. Fahle,et al.  Effects of biased feedback on learning and deciding in a vernier discrimination task , 1999, Vision Research.

[29]  M. Shadlen,et al.  Effect of Expected Reward Magnitude on the Response of Neurons in the Dorsolateral Prefrontal Cortex of the Macaque , 1999, Neuron.

[30]  Steven R. Holloway,et al.  Seeing what is not there shows the costs of perceptual learning. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[31]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[32]  Barbara Anne Dosher,et al.  Independent perceptual learning in monocular and binocular motion systems. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. O'Doherty,et al.  Predictive Neural Coding of Reward Preference Involves Dissociable Responses in Human Ventral Midbrain and Ventral Striatum , 2006, Neuron.

[34]  I. Fujita,et al.  Disparity selectivity of neurons in monkey inferior temporal cortex. , 2000, Journal of neurophysiology.

[35]  Steven R. Holloway,et al.  Perceptual Learning of Motion Leads to Faster Flicker Perception , 2006, PloS one.

[36]  David A. Leopold,et al.  What is rivalling during binocular rivalry? , 1996, Nature.

[37]  G. Orban,et al.  Practising orientation identification improves orientation coding in V1 neurons , 2001, Nature.

[38]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[39]  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.

[40]  K. Nakayama,et al.  Subjective contours, tilt aftereffects, and visual cortical organization , 1989, Vision Research.

[41]  P. Dayan,et al.  Reward, Motivation, and Reinforcement Learning , 2002, Neuron.

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

[43]  O. Hikosaka,et al.  Feature-Based Anticipation of Cues that Predict Reward in Monkey Caudate Nucleus , 2002, Neuron.

[44]  W. Skrandies,et al.  Human perceptual learning in the peripheral visual field: sensory thresholds and neurophysiological correlates , 2002, Biological Psychology.

[45]  Z L Lu,et al.  Perceptual learning reflects external noise filtering and internal noise reduction through channel reweighting. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Katsumi Aoki,et al.  Recent development of flow visualization , 2004, J. Vis..

[47]  R. Dolan,et al.  Subliminal Instrumental Conditioning Demonstrated in the Human Brain , 2008, Neuron.

[48]  Pieter R. Roelfsema,et al.  Attention-Gated Reinforcement Learning of Internal Representations for Classification , 2005, Neural Computation.

[49]  W. Schultz.  Behavioral theories and the neurophysiology of reward. , 2006, Annual review of psychology.

[50]  T. Poggio,et al.  Fast perceptual learning in hyperacuity , 1995, Vision Research.

[51]  T. Robbins,et al.  Distinct Changes in Cortical Acetylcholine and Noradrenaline Efflux during Contingent and Noncontingent Performance of a Visual Attentional Task , 2001, Journal of Neuroscience.

[52]  J. Pearce,et al.  Theories of associative learning in animals. , 2001, Annual review of psychology.

[53]  Aaron R. Seitz,et al.  A unified model for perceptual learning , 2005, Trends in Cognitive Sciences.

[54]  M. Grabowecky,et al.  Long-Term Speeding in Perceptual Switches Mediated by Attention-Dependent Plasticity in Cortical Visual Processing , 2007, Neuron.

[55]  N. Dupuis-Roy,et al.  Perceptual learning without signal , 2007, Vision Research.

[56]  M. Fahle,et al.  The role of feedback in learning a vernier discrimination task , 1997, Vision Research.

[57]  A. Mitz.  A liquid-delivery device that provides precise reward control for neurophysiological and behavioral experiments , 2005, Journal of Neuroscience Methods.