A Recurrent Neural Network Based Model of Predictive Smooth Pursuit Eye Movement in Primates

A predictive mechanism in the brain enables primates to visually track a target with almost zero lag smooth pursuit eye movements, overcoming the delays in processing retinal inputs. Interestingly, it also allows pursuit of occluded targets with nonlinear motion patterns. We propose a recurrent neural network (RNN) model that rapidly learns the target velocity sequence and generates eye velocity signals to eliminate the initial lag between target and eye velocities, and to track occluded targets with nonlinear velocity. Moreover, the model is able to adapt to unpredictable perturbation and phase shift of target velocity and qualitatively reproduce the initial pursuit acceleration in experimentally observed timescales. We propose that the frontal eye field (FEF) region of the primate brain is homologous to the proposed RNN based on its persistent predictive activities during pursuit and location on the pursuit pathway.

[1]  G. Barnes,et al.  Predictive velocity estimation in the pursuit reflex response to pseudo‐random and step displacement stimuli in man. , 1987, The Journal of physiology.

[2]  E. G. Keating,et al.  Frontal eye field lesions impair predictive and visually-guided pursuit eye movements , 2004, Experimental Brain Research.

[3]  Stefan Schaal,et al.  A model of smooth pursuit in primates based on learning the target dynamics , 2005, Neural Networks.

[4]  S. Whittaker,et al.  Learning patterns of eye motion for foveal pursuit. , 1982, Investigative ophthalmology & visual science.

[5]  W. Bialek,et al.  A sensory source for motor variation , 2005, Nature.

[6]  Stephen G. Lisberger,et al.  A model of visually-guided smooth pursuit eye movements based on behavioral observations , 1994, Journal of Computational Neuroscience.

[7]  Simon J. Bennett,et al.  Smooth ocular pursuit during the transient disappearance of an accelerating visual target: the role of reflexive and voluntary control , 2006, Experimental Brain Research.

[8]  C. Bruce,et al.  Smooth-pursuit eye movement representation in the primate frontal eye field. , 1991, Cerebral cortex.

[9]  F. Binkofski,et al.  Cortical mechanisms of smooth pursuit eye movements with target blanking. An fMRI study , 2004, The European journal of neuroscience.

[10]  A. V. van den Berg,et al.  Human smooth pursuit during transient perturbations of predictable and unpredictable target movement , 2004, Experimental Brain Research.

[11]  Jean-Jacques Orban de Xivry,et al.  Kalman Filtering Naturally Accounts for Visually Guided and Predictive Smooth Pursuit Dynamics , 2013, The Journal of Neuroscience.

[12]  S. G. Wells,et al.  Elling Prediction in Ocular Pursuit , 1999 .

[13]  Manfred Mackeben,et al.  Pursuit eye movements and their neural control in the monkey , 1978, Pflügers Archiv.

[14]  W. Maass,et al.  Self-tuning of neural circuits through short-term synaptic plasticity. , 2007, Journal of neurophysiology.

[15]  Yu Zhao,et al.  Intrinsically motivated learning of visual motion perception and smooth pursuit , 2014, 2014 IEEE International Conference on Robotics and Automation (ICRA).

[16]  Yu Zhao,et al.  Self-calibrating smooth pursuit through active efficient coding , 2015, Robotics Auton. Syst..

[17]  D S Zee,et al.  Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit. , 2000, Journal of neurophysiology.

[18]  M. Missal,et al.  Quantitative analysis of catch-up saccades during sustained pursuit. , 2002, Journal of neurophysiology.

[19]  K. Fukushima,et al.  Predictive responses of periarcuate pursuit neurons to visual target motion , 2002, Experimental Brain Research.

[20]  A. Terry Bahill,et al.  Model emulates human smooth pursuit system producing zero-latency target tracking , 1983, Biological Cybernetics.

[21]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[22]  S. Yasui,et al.  On the predictive control of foveal eye tracking and slow phases of optokinetic and vestibular nystagmus. , 1984, The Journal of physiology.

[23]  Herbert Jaeger,et al.  The''echo state''approach to analysing and training recurrent neural networks , 2001 .

[24]  R. Andersen Visual and eye movement functions of the posterior parietal cortex. , 1989, Annual review of neuroscience.

[25]  L. F. Abbott,et al.  Generating Coherent Patterns of Activity from Chaotic Neural Networks , 2009, Neuron.

[26]  Stephen G Lisberger,et al.  Encoding and decoding of learned smooth-pursuit eye movements in the floccular complex of the monkey cerebellum. , 2009, Journal of neurophysiology.

[27]  Henry Markram,et al.  Real-Time Computing Without Stable States: A New Framework for Neural Computation Based on Perturbations , 2002, Neural Computation.

[28]  Karl R. Gegenfurtner,et al.  Precision of speed discrimination and smooth pursuit eye movements , 2009, Vision Research.

[29]  G. Barnes,et al.  Cognitive processes involved in smooth pursuit eye movements , 2008, Brain and Cognition.

[30]  Karl R Gegenfurtner,et al.  Contextual effects on smooth-pursuit eye movements. , 2007, Journal of neurophysiology.

[31]  E. J. Morris,et al.  Visual motion processing and sensory-motor integration for smooth pursuit eye movements. , 1987, Annual review of neuroscience.

[32]  Christopher C. Pack,et al.  A Neural Model of Smooth Pursuit Control and Motion Perception by Cortical Area MST , 2001, Journal of Cognitive Neuroscience.

[33]  J. L. Gordon,et al.  A model of the smooth pursuit eye movement system , 1986, Biological Cybernetics.

[34]  H. Collewijn,et al.  Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. , 1984, The Journal of physiology.

[35]  E. Keller,et al.  Characterization of prediction in the primate visual smooth pursuit system. , 1995, Bio Systems.

[36]  M. Kawato,et al.  Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum , 1993, Nature.