A model of visual–spatial memory across saccades

This paper describes a neural network model that directs saccades back to targets after they disappear and other saccades intervene. This is a simple example of knowing where something is after it is no longer visible and the observer has moved. These tasks require a short-term memory that can store continuous values of spatial location. The model was generated by training a neural network with a recurrently connected hidden layer to specify memory-guided saccades. The trained network maintains stored locations accurately for a few seconds. It uses a leaky integrator mechanism in which there is a slow decay of the stored value to a small number of fixed point attractors. Similar mechanisms have been used to model oculomotor integration (Cannon, S., Robinson, D., & Shamma, S. (1983). A proposed neural network for the integrator of the oculomotor system. Biological Cybernetics, 49, 127-136; Seung, H. (1998). Continuous attractors and oculomotor control. Neural Networks, 11, 1253-1258). The mechanism is robust to parameters such as the input and output format and the constraints in training. However, the receptive field properties of the hidden units do depend on these parameters. It was possible to find biologically plausible parameters that produced hidden unit behavior similar to that of real neurons involved in saccade memory. In particular, training the model to simultaneously represent the target location in both eye- and head-based reference frames produces units similar to neurons in parietal saccade areas.

[1]  L E Mays,et al.  Saccades are spatially, not retinocentrically, coded. , 1980, Science.

[2]  Geoffrey E. Hinton,et al.  Learning internal representations by error propagation , 1986 .

[3]  J. Gnadt,et al.  Statistical Analysis of the Information Content in the Activity of Cortical Neurons , 1996, Vision Research.

[4]  T. L. Harrington,et al.  Neural mechanisms of space vision in the parietal association cortex of the monkey , 1985, Vision Research.

[5]  Lawrence E Mays,et al.  Neuronal circuitry controlling the near response , 1995, Current Opinion in Neurobiology.

[6]  Ronald J. Williams,et al.  Gradient-based learning algorithms for recurrent networks and their computational complexity , 1995 .

[7]  D. Sparks The neural encoding of the location of targets for saccadic eye movements. , 1989, The Journal of experimental biology.

[8]  Richard A. Andersen,et al.  A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons , 1988, Nature.

[9]  H. Sakata,et al.  Spatial properties of visual fixation neurons in posterior parietal association cortex of the monkey. , 1980, Journal of neurophysiology.

[10]  David Zipser,et al.  Recurrent Network Model of the Neural Mechanism of Short-Term Active Memory , 1991, Neural Computation.

[11]  A Berthoz,et al.  A neural network model of sensoritopic maps with predictive short-term memory properties. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R. Andersen,et al.  Eye-centered, head-centered, and intermediate coding of remembered sound locations in area LIP. , 1996, Journal of neurophysiology.

[13]  C. C. A. M. Gielen,et al.  Remapping of neural activity in the motor colliculus: A neural network study , 1993, Vision Research.

[14]  L E Mays,et al.  Neurons in monkey parietal area LIP are tuned for eye-movement parameters in three-dimensional space. , 1995, Journal of neurophysiology.

[15]  D. Sparks,et al.  Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. , 1983, Journal of neurophysiology.

[16]  F. Bremmer,et al.  Spatial invarianceof visual receptivefields inparietal cortexneurons , 1997 .

[17]  S. Squatrito,et al.  Gaze field properties of eye position neurones in areas MST and 7a of the macaque monkey , 1996, Visual Neuroscience.

[18]  C. Galletti,et al.  Functional Properties of Neurons in the Anterior Bank of the Parieto‐occipital Sulcus of the Macaque Monkey , 1991, The European journal of neuroscience.

[19]  S L Moody,et al.  A Model That Accounts for Activity in Primate Frontal Cortex during a Delayed Matching-to-Sample Task , 1998, The Journal of Neuroscience.

[20]  R. Andersen,et al.  Posterior parietal cortex. , 1989, Reviews of oculomotor research.

[21]  A. K. Moschovakis,et al.  Neural network simulations of the primate oculomotor system. II. Frames of reference , 1996, Brain Research Bulletin.

[22]  C. Scudder,et al.  The microscopic anatomy and physiology of the mammalian saccadic system , 1996, Progress in Neurobiology.

[23]  Jacqui Lee Schiff,et al.  Frames of Reference , 1975 .

[24]  P. E. Hallett,et al.  Saccadic eye movements towards stimuli triggered by prior saccades , 1976, Vision Research.

[25]  A. John van Opstal,et al.  An Analysis of Craniocentric and Oculocentric Coding Stages in a Neural Network Model of the Saccadic System , 1996, Neural Networks.

[26]  H. Sebastian Seung,et al.  Continuous attractors and oculomotor control , 1998, Neural Networks.

[27]  R. Andersen,et al.  Electrical microstimulation distinguishes distinct saccade-related areas in the posterior parietal cortex. , 1998, Journal of neurophysiology.

[28]  D. Zipser,et al.  Identification models of the nervous system , 1992, Neuroscience.

[29]  R. Baloh,et al.  Quantitative measurement of saccade amplitude, duration, and velocity , 1975, Neurology.

[30]  Paul W. Glimcher,et al.  Response fields of intraparietal neurons quantified with multiple saccadic targets , 1998, Experimental Brain Research.

[31]  Casper J. Erkelens,et al.  Voluntary binocular gaze-shifts in the plane of regard: Dynamics of version and vergence , 1995, Vision Research.

[32]  R. Andersen,et al.  Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque , 1990, The Journal of comparative neurology.

[33]  C. Galletti,et al.  Eye Position Influence on the Parieto‐occipital Area PO (V6) of the Macaque Monkey , 1995, The European journal of neuroscience.

[34]  L. Fogassi,et al.  Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  K. Zhang,et al.  Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  David L. Sparks,et al.  Role of the Monkey Superior Colliculus in the Spatial Localization of Saccade Targets , 1983 .

[37]  D L Sparks,et al.  Spatial localization of saccade targets. II. Activity of superior colliculus neurons preceding compensatory saccades. , 1983, Journal of neurophysiology.