Reinforcement learning can account for associative and perceptual learning on a visual decision task

We recently showed that improved perceptual performance on a visual motion direction–discrimination task corresponds to changes in how an unmodified sensory representation in the brain is interpreted to form a decision that guides behavior. Here we found that these changes can be accounted for using a reinforcement-learning rule to shape functional connectivity between the sensory and decision neurons. We modeled performance on the basis of the readout of simulated responses of direction-selective sensory neurons in the middle temporal area (MT) of monkey cortex. A reward prediction error guided changes in connections between these sensory neurons and the decision process, first establishing the association between motion direction and response direction, and then gradually improving perceptual sensitivity by selectively strengthening the connections from the most sensitive neurons in the sensory population. The results suggest a common, feedback-driven mechanism for some forms of associative and perceptual learning.

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

[2]  P. Anandan,et al.  Pattern-recognizing stochastic learning automata , 1985, IEEE Transactions on Systems, Man, and Cybernetics.

[3]  R. Sekuler,et al.  Direction-specific improvement in motion discrimination , 1987, Vision Research.

[4]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[6]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[7]  David J. Spiegelhalter,et al.  Sequential updating of conditional probabilities on directed graphical structures , 1990, Networks.

[8]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  K. H. Britten,et al.  Responses of neurons in macaque MT to stochastic motion signals , 1993, Visual Neuroscience.

[10]  W. Newsome,et al.  Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[12]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

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

[15]  Haim Sompolinsky,et al.  The Effect of Correlations on the Fisher Information of Population Codes , 1998, NIPS.

[16]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[17]  B. Dosher,et al.  Mechanisms of perceptual learning , 1999, Vision Research.

[18]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[19]  Stefan Treue,et al.  Different populations of neurons contribute to the detection and discrimination of visual motion , 2001, Vision Research.

[20]  M. Merzenich,et al.  Cortical remodelling induced by activity of ventral tegmental dopamine neurons , 2001, Nature.

[21]  H. Sompolinsky,et al.  Population coding in neuronal systems with correlated noise. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  J. Gold,et al.  Neural computations that underlie decisions about sensory stimuli , 2001, Trends in Cognitive Sciences.

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

[24]  W. Bair,et al.  Correlated Firing in Macaque Visual Area MT: Time Scales and Relationship to Behavior , 2001, The Journal of Neuroscience.

[25]  M. Shadlen,et al.  Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task , 2002, The Journal of Neuroscience.

[26]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[27]  S. Royer,et al.  Conservation of total synaptic weight through balanced synaptic depression and potentiation , 2003, Nature.

[28]  J. Gold,et al.  The Influence of Behavioral Context on the Representation of a Perceptual Decision in Developing Oculomotor Commands , 2003, The Journal of Neuroscience.

[29]  M. Shadlen,et al.  A role for neural integrators in perceptual decision making. , 2003, Cerebral cortex.

[30]  Ronald J. Williams,et al.  Simple Statistical Gradient-Following Algorithms for Connectionist Reinforcement Learning , 2004, Machine Learning.

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

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

[33]  D. Bradley,et al.  Neural population code for fine perceptual decisions in area MT , 2005, Nature Neuroscience.

[34]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

[35]  K. Berridge The debate over dopamine’s role in reward: the case for incentive salience , 2007, Psychopharmacology.

[36]  Yonatan Loewenstein,et al.  Operant matching is a generic outcome of synaptic plasticity based on the covariance between reward and neural activity , 2006, Proceedings of the National Academy of Sciences.

[37]  C. Carter,et al.  Error Detection, Correction, and Prevention in the Brain: A Brief Review of Data and Theories , 2006, Clinical EEG and neuroscience.

[38]  Timothy D. Hanks,et al.  Microstimulation of macaque area LIP affects decision-making in a motion discrimination task , 2006, Nature Neuroscience.

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

[40]  J. Movshon,et al.  A new perceptual illusion reveals mechanisms of sensory decoding , 2007, Nature.

[41]  Ikuko Mukai,et al.  Activations in Visual and Attention-Related Areas Predict and Correlate with the Degree of Perceptual Learning , 2007, The Journal of Neuroscience.

[42]  W. Schultz Multiple dopamine functions at different time courses. , 2007, Annual review of neuroscience.

[43]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[44]  Timothy D. Hanks,et al.  Bounded Integration in Parietal Cortex Underlies Decisions Even When Viewing Duration Is Dictated by the Environment , 2008, The Journal of Neuroscience.

[45]  P. Redgrave,et al.  What is reinforced by phasic dopamine signals? , 2008, Brain Research Reviews.

[46]  Hatim A. Zariwala,et al.  Neural correlates, computation and behavioural impact of decision confidence , 2008, Nature.

[47]  P. Dayan,et al.  Decision theory, reinforcement learning, and the brain , 2008, Cognitive, affective & behavioral neuroscience.

[48]  C. Law,et al.  Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area , 2008, Nature Neuroscience.

[49]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque , 2008 .

[50]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.

[51]  Joshua I Gold,et al.  Correlates of Perceptual Learning in an Oculomotor Decision Variable , 2009, The Journal of Neuroscience.

[52]  R. K. Simpson Nature Neuroscience , 2022 .