Itinerancy between attractor states in neural systems

Converging evidence from neural, perceptual and simulated data suggests that discrete attractor states form within neural circuits through learning and development. External stimuli may bias neural activity to one attractor state or cause activity to transition between several discrete states. Evidence for such transitions, whose timing can vary across trials, is best accrued through analyses that avoid any trial-averaging of data. One such method, hidden Markov modeling, has been effective in this context, revealing state transitions in many neural circuits during many tasks. Concurrently, modeling efforts have revealed computational benefits of stimulus processing via transitions between attractor states. This review describes the current state of the field, with comments on how its perceived limitations have been addressed.

[1]  Walter J. Freeman,et al.  Metastability, instability, and state transition in neocortex , 2005, Neural Networks.

[2]  D. Durstewitz,et al.  Beyond bistability: Biophysics and temporal dynamics of working memory , 2006, Neuroscience.

[3]  Paul Miller,et al.  Stabilization of Memory States by Stochastic Facilitating Synapses , 2013, Journal of mathematical neuroscience.

[4]  Sandro Romani,et al.  Scaling Laws of Associative Memory Retrieval , 2013, Neural Computation.

[5]  Earl K. Miller,et al.  Neural ensemble states in prefrontal cortex identified using a hidden Markov model with a modified EM algorithm , 2000, Neurocomputing.

[6]  Martin Golubitsky,et al.  What Geometric Visual Hallucinations Tell Us about the Visual Cortex , 2002, Neural Computation.

[7]  Sang-Hee Lee,et al.  Characterization of the crawling activity of Caenorhabditis elegans using a hidden markov model , 2015, Theory in Biosciences.

[8]  György Buzsáki,et al.  Neural Syntax: Cell Assemblies, Synapsembles, and Readers , 2010, Neuron.

[9]  S Grossberg,et al.  Some nonlinear networks capable of learning a spatial pattern of arbitrary complexity. , 1968, Proceedings of the National Academy of Sciences of the United States of America.

[10]  József Fiser,et al.  Spontaneous Cortical Activity Reveals Hallmarks of an Optimal Internal Model of the Environment , 2011, Science.

[11]  D. Durstewitz,et al.  Abrupt Transitions between Prefrontal Neural Ensemble States Accompany Behavioral Transitions during Rule Learning , 2010, Neuron.

[12]  Theo Geisel,et al.  Uncovering the synchronization dynamics from correlated neuronal activity quantifies assembly formation , 1994, Biological Cybernetics.

[13]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[14]  Paul Miller,et al.  Distinct Effects of Perceptual Quality on Auditory Word Recognition, Memory Formation and Recall in a Neural Model of Sequential Memory , 2010, Front. Syst. Neurosci..

[15]  Paul Miller,et al.  Accuracy and response-time distributions for decision-making: linear perfect integrators versus nonlinear attractor-based neural circuits , 2013, Journal of Computational Neuroscience.

[16]  Paul Miller,et al.  Stability of discrete memory states to stochastic fluctuations in neuronal systems. , 2006, Chaos.

[17]  Nao Ninomiya,et al.  The 10th anniversary of journal of visualization , 2007, J. Vis..

[18]  Alberto Bernacchia,et al.  The interplay of plasticity and adaptation in neural circuits: a generative model , 2014, Front. Synaptic Neurosci..

[19]  Y. Niv,et al.  The effects of motivation on response rate: A hidden semi-Markov model analysis of behavioral dynamics , 2011, Journal of Neuroscience Methods.

[20]  Stiliyan Kalitzin,et al.  Multiple oscillatory States in Models of Collective neuronal Dynamics , 2014, Int. J. Neural Syst..

[21]  G. La Camera,et al.  Dynamics of Multistable States during Ongoing and Evoked Cortical Activity , 2015, The Journal of Neuroscience.

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

[23]  E. Seidemann,et al.  Simultaneously recorded single units in the frontal cortex go through sequences of discrete and stable states in monkeys performing a delayed localization task , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[25]  Xiao-Jing Wang,et al.  A Recurrent Network Mechanism of Time Integration in Perceptual Decisions , 2006, The Journal of Neuroscience.

[26]  Naftali Tishby,et al.  Cortical activity flips among quasi-stationary states. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[27]  P. J. Sjöström,et al.  Functional specificity of local synaptic connections in neocortical networks , 2011, Nature.

[28]  David Kappel,et al.  STDP Installs in Winner-Take-All Circuits an Online Approximation to Hidden Markov Model Learning , 2014, PLoS Comput. Biol..

[29]  Gustavo Deco,et al.  Functional connectivity dynamics: Modeling the switching behavior of the resting state , 2015, NeuroImage.

[30]  Ichiro Tsuda,et al.  Chaotic itinerancy and its roles in cognitive neurodynamics , 2015, Current Opinion in Neurobiology.

[31]  Valentin Afraimovich,et al.  Sequential memory: Binding dynamics. , 2015, Chaos.

[32]  B. McNaughton,et al.  Paradoxical Effects of External Modulation of Inhibitory Interneurons , 1997, The Journal of Neuroscience.

[33]  Sandro Romani,et al.  Neural Network Model of Memory Retrieval , 2015, Front. Comput. Neurosci..

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

[35]  Nava Rubin,et al.  Alternation rate in perceptual bistability is maximal at and symmetric around equi-dominance. , 2010, Journal of vision.

[36]  Naftali Tishby,et al.  Hidden Markov modelling of simultaneously recorded cells in the associative cortex of behaving monkeys , 1997 .

[37]  A. Treves,et al.  Neural attractor dynamics in object recognition , 2010, Experimental Brain Research.

[38]  Alessandro Treves,et al.  Frontal latching networks: a possible neural basis for infinite recursion , 2005, Cognitive neuropsychology.

[39]  Itamar Lerner,et al.  Integrating the Automatic and the Controlled: Strategies in Semantic Priming in an Attractor Network With Latching Dynamics , 2014, Cogn. Sci..

[40]  M. Carandini,et al.  Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. , 2000, Journal of neurophysiology.

[41]  Henry Markram,et al.  Computing the size and number of neuronal clusters in local circuits , 2013, Front. Neuroanat..

[42]  Wolfgang Maass,et al.  Emergence of Dynamic Memory Traces in Cortical Microcircuit Models through STDP , 2013, The Journal of Neuroscience.

[43]  Alessandro Treves,et al.  Cortical free-association dynamics: distinct phases of a latching network. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[44]  Robert Kozma,et al.  Robust sequential working memory recall in heterogeneous cognitive networks , 2014, Front. Syst. Neurosci..

[45]  Viktor K. Jirsa,et al.  Multistability in Large Scale Models of Brain Activity , 2013, BMC Neuroscience.

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

[47]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[48]  Peter E. Latham,et al.  Computing and Stability in Cortical Networks , 2004, Neural Computation.

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

[50]  Pablo Varona,et al.  Chunking dynamics: heteroclinics in mind , 2014, Front. Comput. Neurosci..

[51]  KongFatt Wong-Lin,et al.  Neural Circuit Dynamics Underlying Accumulation of Time-Varying Evidence During Perceptual Decision Making , 2007, Frontiers Comput. Neurosci..

[52]  P. Miller,et al.  Stochastic Transitions between Neural States in Taste Processing and Decision-Making , 2010, The Journal of Neuroscience.

[53]  E. Miller,et al.  Task-Dependent Changes in Short-Term Memory in the Prefrontal Cortex , 2010, The Journal of Neuroscience.

[54]  A. Treves,et al.  Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain , 2005, Nature Neuroscience.

[55]  A. Litwin-Kumar,et al.  Formation and maintenance of neuronal assemblies through synaptic plasticity , 2014, Nature Communications.

[56]  Mikhail Rabinovich,et al.  Learning of Chunking Sequences in Cognition and Behavior , 2015, PLoS Comput. Biol..

[57]  G. Deco,et al.  Ongoing Cortical Activity at Rest: Criticality, Multistability, and Ghost Attractors , 2012, The Journal of Neuroscience.

[58]  Xiao-Jing Wang Decision Making in Recurrent Neuronal Circuits , 2008, Neuron.

[59]  A. Litwin-Kumar,et al.  Slow dynamics and high variability in balanced cortical networks with clustered connections , 2012, Nature Neuroscience.

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

[61]  G. Radons,et al.  Analysis, classification, and coding of multielectrode spike trains with hidden Markov models , 2004, Biological Cybernetics.

[62]  Daniel J. Amit,et al.  Mean Field and Capacity in Realistic Networks of Spiking Neurons Storing Sparsely Coded Random Memories , 2004, Neural Computation.

[63]  Liam Paninski,et al.  Hidden Markov Models for the Stimulus-Response Relationships of Multistate Neural Systems , 2011, Neural Computation.

[64]  J. R. Otterpohl,et al.  Extracting the dynamics of perceptual switching from ‘noisy’ behaviour: An application of hidden Markov modelling to pecking data from pigeons , 2000, Journal of Physiology-Paris.

[65]  Gustavo Deco,et al.  Neural Network Mechanisms Underlying Stimulus Driven Variability Reduction , 2012, PLoS Comput. Biol..

[66]  J. Rinzel,et al.  Noise-induced alternations in an attractor network model of perceptual bistability. , 2007, Journal of neurophysiology.

[67]  Brent Doiron,et al.  Balanced neural architecture and the idling brain , 2014, Front. Comput. Neurosci..

[68]  A Treves,et al.  Associative memory neural network with low temporal spiking rates. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Yoram Burak,et al.  Fundamental limits on persistent activity in networks of noisy neurons , 2012, Proceedings of the National Academy of Sciences.

[70]  Alessandro Treves,et al.  The storage capacity of Potts models for semantic memory retrieval , 2005 .

[71]  Paul Miller,et al.  Dynamical systems, attractors, and neural circuits , 2016, F1000Research.

[72]  M. Kringelbach,et al.  The Rediscovery of Slowness: Exploring the Timing of Cognition , 2015, Trends in Cognitive Sciences.

[73]  I. Tsuda Toward an interpretation of dynamic neural activity in terms of chaotic dynamical systems. , 2001, The Behavioral and brain sciences.

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

[76]  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.

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

[78]  Mauricio Barahona,et al.  Emergence of Slow-Switching Assemblies in Structured Neuronal Networks , 2015, PLoS Comput. Biol..

[79]  Paul Miller,et al.  Excitatory, Inhibitory, and Structural Plasticity Produce Correlated Connectivity in Random Networks Trained to Solve Paired-Stimulus Tasks , 2011, Front. Comput. Neurosci..

[80]  Alessandro Treves,et al.  Stable and Rapid Recurrent Processing in Realistic Autoassociative Memories , 1998, Neural Computation.

[81]  Gustavo Deco,et al.  Networks for memory, perception, and decision-making, and beyond to how the syntax for language might be implemented in the brain , 2015, Brain Research.

[82]  X. Wang,et al.  Synaptic Basis of Cortical Persistent Activity: the Importance of NMDA Receptors to Working Memory , 1999, The Journal of Neuroscience.

[83]  Albert Goldbeter,et al.  Circadian rhythms and molecular noise. , 2006, Chaos.

[84]  J J Hopfield,et al.  Neurons with graded response have collective computational properties like those of two-state neurons. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[85]  Paul Miller,et al.  Natural stimuli evoke dynamic sequences of states in sensory cortical ensembles , 2007, Proceedings of the National Academy of Sciences.

[86]  D. Knill,et al.  Bayesian sampling in visual perception , 2011, Proceedings of the National Academy of Sciences.

[87]  L. Abbott,et al.  From fixed points to chaos: Three models of delayed discrimination , 2013, Progress in Neurobiology.

[88]  A. Grinvald,et al.  Spontaneously emerging cortical representations of visual attributes , 2003, Nature.

[89]  Treves,et al.  Graded-response neurons and information encodings in autoassociative memories. , 1990, Physical review. A, Atomic, molecular, and optical physics.

[90]  P. Miller,et al.  The Behavioral Relevance of Cortical Neural Ensemble Responses Emerges Suddenly , 2016, The Journal of Neuroscience.

[91]  Y. Miyashita Neuronal correlate of visual associative long-term memory in the primate temporal cortex , 1988, Nature.

[92]  H Sompolinsky,et al.  Dynamics of random neural networks with bistable units. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[93]  W. Freeman,et al.  Chaotic Oscillations and the Genesis of Meaning in Cerebral Cortex , 1994 .

[94]  W J Freeman,et al.  Characterization of state transitions in spatially distributed, chaotic, nonlinear, dynamical systems in cerebral cortex , 1994, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[95]  Wolfgang Maass,et al.  Bayesian Computation Emerges in Generic Cortical Microcircuits through Spike-Timing-Dependent Plasticity , 2013, PLoS Comput. Biol..

[96]  R. Romo,et al.  Dynamics of Cortical Neuronal Ensembles Transit from Decision Making to Storage for Later Report , 2012, The Journal of Neuroscience.

[97]  Thomas K. Berger,et al.  A synaptic organizing principle for cortical neuronal groups , 2011, Proceedings of the National Academy of Sciences.

[98]  C. Snowdon Response of nonhuman animals to speech and to species-specific sounds. , 1979, Brain, behavior and evolution.

[99]  Haim Sompolinsky,et al.  Patterns of Ongoing Activity and the Functional Architecture of the Primary Visual Cortex , 2004, Neuron.

[100]  Paul Miller,et al.  Stimulus number, duration and intensity encoding in randomly connected attractor networks with synaptic depression , 2013, Front. Comput. Neurosci..

[101]  Sompolinsky,et al.  Willshaw model: Associative memory with sparse coding and low firing rates. , 1990, Physical review. A, Atomic, molecular, and optical physics.

[102]  A. Grinvald,et al.  Linking spontaneous activity of single cortical neurons and the underlying functional architecture. , 1999, Science.

[103]  Tomoki Fukai,et al.  Temporal integration by stochastic recurrent network dynamics with bimodal neurons. , 2007, Journal of neurophysiology.

[104]  J. Fuster,et al.  Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. , 1981, Science.

[105]  Masato Okada,et al.  Complex Sequencing Rules of Birdsong Can be Explained by Simple Hidden Markov Processes , 2010, PloS one.

[106]  Robert A. Legenstein,et al.  Ensembles of Spiking Neurons with Noise Support Optimal Probabilistic Inference in a Dynamically Changing Environment , 2014, PLoS Comput. Biol..

[107]  Athena Akrami,et al.  Lateral thinking, from the Hopfield model to cortical dynamics , 2012, Brain Research.

[108]  Jonathan W. Pillow,et al.  Single-trial spike trains in parietal cortex reveal discrete steps during decision-making , 2015, Science.

[109]  Daniel B. Rubin,et al.  The Stabilized Supralinear Network: A Unifying Circuit Motif Underlying Multi-Input Integration in Sensory Cortex , 2015, Neuron.

[110]  Sandro Romani,et al.  Effects of long-term representations on free recall of unrelated words , 2015, Learning & memory.

[111]  Sandro Romani,et al.  Word length effect in free recall of randomly assembled word lists , 2014, Front. Comput. Neurosci..

[112]  J. Ditterich,et al.  Neural Dynamics of Choice: Single-Trial Analysis of Decision-Related Activity in Parietal Cortex , 2012, The Journal of Neuroscience.

[113]  E. Rolls,et al.  Stochastic cortical neurodynamics underlying the memory and cognitive changes in aging , 2015, Neurobiology of Learning and Memory.

[114]  Nava Rubin,et al.  Balance between noise and adaptation in competition models of perceptual bistability , 2009, Journal of Computational Neuroscience.

[115]  Leslie M Kay,et al.  Granule cell excitability regulates gamma and beta oscillations in a model of the olfactory bulb dendrodendritic microcircuit. , 2016, Journal of neurophysiology.

[116]  E. Marder,et al.  Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. , 1991, Journal of neurophysiology.

[117]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.