Continuous Attractors with Morphed/Correlated Maps

Continuous attractor networks are used to model the storage and representation of analog quantities, such as position of a visual stimulus. The storage of multiple continuous attractors in the same network has previously been studied in the context of self-position coding. Several uncorrelated maps of environments are stored in the synaptic connections, and a position in a given environment is represented by a localized pattern of neural activity in the corresponding map, driven by a spatially tuned input. Here we analyze networks storing a pair of correlated maps, or a morph sequence between two uncorrelated maps. We find a novel state in which the network activity is simultaneously localized in both maps. In this state, a fixed cue presented to the network does not determine uniquely the location of the bump, i.e. the response is unreliable, with neurons not always responding when their preferred input is present. When the tuned input varies smoothly in time, the neuronal responses become reliable and selective for the environment: the subset of neurons responsive to a moving input in one map changes almost completely in the other map. This form of remapping is a non-trivial transformation between the tuned input to the network and the resulting tuning curves of the neurons. The new state of the network could be related to the formation of direction selectivity in one-dimensional environments and hippocampal remapping. The applicability of the model is not confined to self-position representations; we show an instance of the network solving a simple delayed discrimination task.

[1]  Alessandro Treves,et al.  The CA3 network as a memory store for spatial representations. , 2007, Learning & memory.

[2]  M. Tsodyks,et al.  Synaptic Theory of Working Memory , 2008, Science.

[3]  Mark C. Fuhs,et al.  A Spin Glass Model of Path Integration in Rat Medial Entorhinal Cortex , 2006, The Journal of Neuroscience.

[4]  J. Cowan,et al.  A mathematical theory of visual hallucination patterns , 1979, Biological Cybernetics.

[5]  S. Amari Dynamics of pattern formation in lateral-inhibition type neural fields , 1977, Biological Cybernetics.

[6]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[7]  Mark C. W. van Rossum,et al.  Recurrent networks with short term synaptic depression , 2009, Journal of Computational Neuroscience.

[8]  B L McNaughton,et al.  Path Integration and Cognitive Mapping in a Continuous Attractor Neural Network Model , 1997, The Journal of Neuroscience.

[9]  M. Moser,et al.  Understanding memory through hippocampal remapping , 2008, Trends in Neurosciences.

[10]  D. Sagi,et al.  Dynamics of Memory Representations in Networks with Novelty-Facilitated Synaptic Plasticity , 2006, Neuron.

[11]  Li I. Zhang,et al.  Topography and synaptic shaping of direction selectivity in primary auditory cortex , 2003, Nature.

[12]  Alessandro Treves,et al.  Attractor neural networks storing multiple space representations: A model for hippocampal place fields , 1998, cond-mat/9807101.

[13]  J. Cowan,et al.  A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue , 1973, Kybernetik.

[14]  B. McNaughton,et al.  Population dynamics and theta rhythm phase precession of hippocampal place cell firing: A spiking neuron model , 1998, Hippocampus.

[15]  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.

[16]  R. Romo,et al.  Neuronal Population Coding of Parametric Working Memory , 2010, The Journal of Neuroscience.

[17]  Terrence J. Sejnowski,et al.  ASSOCIATIVE MEMORY AND HIPPOCAMPAL PLACE CELLS , 1995 .

[18]  B. Ermentrout Neural networks as spatio-temporal pattern-forming systems , 1998 .

[19]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Yoram Burakyy,et al.  Accurate Path Integration in Continuous Attractor Network Models of Grid Cells , 2009 .

[21]  N. Rashevsky,et al.  Mathematical biology , 1961, Connecticut medicine.

[22]  M. Fyhn,et al.  Spatial Representation in the Entorhinal Cortex , 2004, Science.

[23]  A David Redishyx,et al.  A coupled attractor model of the rodent head direction system , 1996 .

[24]  Neil Burgess,et al.  Attractor Dynamics in the Hippocampal Representation of the Local Environment , 2005, Science.

[25]  Daniel J. Amit,et al.  Modeling brain function: the world of attractor neural networks, 1st Edition , 1989 .

[26]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[27]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Henry Markram,et al.  Neural Networks with Dynamic Synapses , 1998, Neural Computation.

[29]  Bruce L. McNaughton,et al.  Progressive Transformation of Hippocampal Neuronal Representations in “Morphed” Environments , 2005, Neuron.

[30]  H S Seung,et al.  How the brain keeps the eyes still. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[31]  K. Tanaka,et al.  Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[32]  Alberto Bernacchia,et al.  Impact of spatiotemporally correlated images on the structure of memory , 2007, Proceedings of the National Academy of Sciences.

[33]  Daniel D. Lee,et al.  Stability of the Memory of Eye Position in a Recurrent Network of Conductance-Based Model Neurons , 2000, Neuron.

[34]  Alessandro Treves,et al.  Representing Where along with What Information in a Model of a Cortical Patch , 2008, PLoS Comput. Biol..

[35]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[36]  R. Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  Idan Segev,et al.  Methods in Neuronal Modeling , 1988 .

[38]  Misha Tsodyks,et al.  The effects of perceptual history on memory of visual objects , 2007, Vision Research.

[39]  H. C. LONGUET-HIGGINS,et al.  Non-Holographic Associative Memory , 1969, Nature.

[40]  Misha Tsodyks,et al.  Correction: Persistent Activity in Neural Networks with Dynamic Synapses , 2007, PLoS Comput. Biol..

[41]  Shun-ichi Amari,et al.  Learning Patterns and Pattern Sequences by Self-Organizing Nets of Threshold Elements , 1972, IEEE Transactions on Computers.

[42]  W E Skaggs,et al.  Deciphering the hippocampal polyglot: the hippocampus as a path integration system. , 1996, The Journal of experimental biology.

[43]  Thomas P. Trappenberg,et al.  Self-organising continuous attractor networks with multiple activity packets, and the representation of space , 2004, Neural Networks.

[44]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M Tsodyks,et al.  Attractor neural network models of spatial maps in hippocampus , 1999, Hippocampus.

[46]  Misha Tsodyks,et al.  From , 2020, Definitions.

[47]  B. McNaughton,et al.  Local Sensory Cues and Place Cell Directionality: Additional Evidence of Prospective Coding in the Hippocampus , 2004, The Journal of Neuroscience.

[48]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[50]  Daniel J. Amit,et al.  Mean-field analysis of selective persistent activity in presence of short-term synaptic depression , 2006, Journal of Computational Neuroscience.

[51]  A. Treves,et al.  Hippocampal remapping and grid realignment in entorhinal cortex , 2007, Nature.