Learning to Attend: Modeling the Shaping of Selectivity in Infero-temporal Cortex in a Categorization Task

Recent experiments on behaving monkeys have shown that learning a visual categorization task makes the neurons in infero-temporal cortex (ITC) more selective to the task-relevant features of the stimuli (Sigala and Logothetis in Nature 415 318–320, 2002). We hypothesize that such a selectivity modulation emerges from the interaction between ITC and other cortical area, presumably the prefrontal cortex (PFC), where the previously learned stimulus categories are encoded. We propose a biologically inspired model of excitatory and inhibitory spiking neurons with plastic synapses, modified according to a reward based Hebbian learning rule, to explain the experimental results and test the validity of our hypothesis. We assume that the ITC neurons, receiving feature selective inputs, form stronger connections with the category specific neurons to which they are consistently associated in rewarded trials. After learning, the top-down influence of PFC neurons enhances the selectivity of the ITC neurons encoding the behaviorally relevant features of the stimuli, as observed in the experiments. We conclude that the perceptual representation in visual areas like ITC can be strongly affected by the interaction with other areas which are devoted to higher cognitive functions.

[1]  Martin Stetter,et al.  Exploration of Cortical Function , 2002, Springer Netherlands.

[2]  Gustavo Deco,et al.  Systems-Level Neuronal Modeling of Visual Attentional Mechanisms , 2003, Artificial Intelligence Review.

[3]  E. Rolls,et al.  What and Where in Visual Working Memory: A Computational Neurodynamical Perspective for Integrating fMRI and Single-Neuron Data , 2004, Journal of Cognitive Neuroscience.

[4]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[5]  John Duncan,et al.  A neural basis for visual search in inferior temporal cortex , 1993, Nature.

[6]  Nicolas Brunel,et al.  Global Spontaneous Activity and Local Structured (learned) Delay Period Activity in Cortex , 1996 .

[7]  Xiao-Jing Wang,et al.  Probabilistic Decision Making by Slow Reverberation in Cortical Circuits , 2002, Neuron.

[8]  Robert L. Goldstone,et al.  Definition , 1960, A Philosopher Looks at Sport.

[9]  P. D. Giudice,et al.  Modelling the formation of working memory with networks of integrate-and-fire neurons connected by plastic synapses , 2003, Journal of Physiology-Paris.

[10]  Gustavo Deco,et al.  A neuronal model for the shaping of feature selectivity in IT by visual categorization , 2005, Neurocomputing.

[11]  Nicolas Brunel,et al.  Dynamics of a recurrent network of spiking neurons before and following learning , 1997 .

[12]  D. Amit,et al.  Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. , 1997, Cerebral cortex.

[13]  KD Miller A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[15]  Daniel J. Amit,et al.  Learning in Neural Networks with Material Synapses , 1994, Neural Computation.

[16]  E W Lang,et al.  Unspecific long‐term potentiation can evoke functional segregation in a model of area 17 , 1998, Neuroreport.

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

[18]  Gustavo Deco,et al.  Modular biased‐competition and cooperation: a candidate mechanism for selective working memory , 2004, The European journal of neuroscience.

[19]  Stefano Fusi,et al.  Hebbian spike-driven synaptic plasticity for learning patterns of mean firing rates , 2002, Biological Cybernetics.

[20]  E. Miller,et al.  Neural Activity in the Primate Prefrontal Cortex during Associative Learning , 1998, Neuron.

[21]  David J. Freedman,et al.  A Comparison of Primate Prefrontal and Inferior Temporal Cortices during Visual Categorization , 2003, The Journal of Neuroscience.

[22]  E. Rolls,et al.  Attention and working memory: a dynamical model of neuronal activity in the prefrontal cortex , 2003, The European journal of neuroscience.

[23]  G. Deco,et al.  Cooperation and biased competition model can explain attentional filtering in the prefrontal cortex , 2004, The European journal of neuroscience.

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

[25]  R. Desimone,et al.  The Role of Neural Mechanisms of Attention in Solving the Binding Problem , 1999, Neuron.

[26]  N. Sigala,et al.  Visual categorization shapes feature selectivity in the primate temporal cortex , 2002, Nature.

[27]  Robert A. Jacobs,et al.  Comparing perceptual learning across tasks: A review , 2002 .

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

[29]  L. Chelazzi Serial attention mechanisms in visual search: A critical look at the evidence , 1999, Psychological research.

[30]  Y. Miyashita,et al.  Top-down signal from prefrontal cortex in executive control of memory retrieval , 1999, Nature.

[31]  Davide Badoni,et al.  Spike-Driven Synaptic Plasticity: Theory, Simulation, VLSI Implementation , 2000, Neural Computation.

[32]  H. Seung,et al.  Learning in Spiking Neural Networks by Reinforcement of Stochastic Synaptic Transmission , 2003, Neuron.

[33]  Müller,et al.  Neural network model for the coordinated formation of orientation preference and orientation selectivity maps. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[34]  Gustavo Deco,et al.  Computational neuroscience of vision , 2002 .