Learning Through Time in the Thalamocortical Loops

We present a comprehensive, novel framework for understanding how the neocortex, including the thalamocortical loops through the deep layers, can support a temporal context representation in the service of predictive learning. Many have argued that predictive learning provides a compelling, powerful source of learning signals to drive the development of human intelligence: if we constantly predict what will happen next, and learn based on the discrepancies from our predictions (error-driven learning), then we can learn to improve our predictions by developing internal representations that capture the regularities of the environment (e.g., physical laws governing the time-evolution of object motions). Our version of this idea builds upon existing work with simple recurrent networks (SRN's), which have a discretely-updated temporal context representations that are a direct copy of the prior internal state representation. We argue that this discretization of temporal context updating has a number of important computational and functional advantages, and further show how the strong alpha-frequency (10hz, 100ms cycle time) oscillations in the posterior neocortex could reflect this temporal context updating. We examine a wide range of data from biology to behavior through the lens of this LeabraTI model, and find that it provides a unified account of a number of otherwise disconnected findings, all of which converge to support this new model of neocortical learning and processing. We describe an implemented model showing how predictive learning of tumbling object trajectories can facilitate object recognition with cluttered backgrounds.

[1]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[2]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[3]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[4]  E. Spelke,et al.  Perception of partly occluded objects in infancy , 1983, Cognitive Psychology.

[5]  Edward M Callaway,et al.  Local connections to specific types of layer 6 neurons in the rat visual cortex. , 2006, Journal of neurophysiology.

[6]  E. Rolls,et al.  INVARIANT FACE AND OBJECT RECOGNITION IN THE VISUAL SYSTEM , 1997, Progress in Neurobiology.

[7]  H. Bülthoff,et al.  What the Human Brain Likes About Facial Motion , 2012, Cerebral cortex.

[8]  Michael I. Jordan Serial Order: A Parallel Distributed Processing Approach , 1997 .

[9]  A. Yuille,et al.  Object perception as Bayesian inference. , 2004, Annual review of psychology.

[10]  Rufin VanRullen,et al.  The Psychophysics of Brain Rhythms , 2011, Front. Psychology.

[11]  R. Luján Exploring the Thalamus and its Role in Cortical Function, S.M. Sherman, R.W. Guillery (Eds.). The MIT Press (2006), ISBN: 0-262-19532-1 , 2007 .

[12]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[13]  Geoffrey E. Hinton,et al.  Reducing the Dimensionality of Data with Neural Networks , 2006, Science.

[14]  K. Mathewson,et al.  Pulsed Out of Awareness: EEG Alpha Oscillations Represent a Pulsed-Inhibition of Ongoing Cortical Processing , 2011, Front. Psychology.

[15]  A. Kleinschmidt,et al.  Modulation of Visually Evoked Cortical fMRI Responses by Phase of Ongoing Occipital Alpha Oscillations , 2011, The Journal of Neuroscience.

[16]  Kuldip K. Paliwal,et al.  Bidirectional recurrent neural networks , 1997, IEEE Trans. Signal Process..

[17]  S. Dalal,et al.  Prestimulus Oscillatory Phase at 7 Hz Gates Cortical Information Flow and Visual Perception , 2013, Current Biology.

[18]  B. Ross,et al.  Beta and Gamma Rhythms in Human Auditory Cortex during Musical Beat Processing , 2009, Annals of the New York Academy of Sciences.

[19]  Geoffrey E. Hinton,et al.  The Helmholtz Machine , 1995, Neural Computation.

[20]  R. O’Reilly,et al.  Computational Explorations in Cognitive Neuroscience: Understanding the Mind by Simulating the Brain , 2000 .

[21]  Tsunehiro Takeda,et al.  Alpha band amplification during illusory jitter perception. , 2008, Journal of vision.

[22]  Nathan Intrator,et al.  Theory of Cortical Plasticity , 2004 .

[23]  R. VanRullen,et al.  The Phase of Ongoing EEG Oscillations Predicts Visual Perception , 2009, The Journal of Neuroscience.

[24]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

[25]  E. Spelke Initial knowledge: six suggestions , 1994, Cognition.

[26]  C. Koch,et al.  Is perception discrete or continuous? , 2003, Trends in Cognitive Sciences.

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

[28]  J. Gross,et al.  Sounds Reset Rhythms of Visual Cortex and Corresponding Human Visual Perception , 2012, Current Biology.

[29]  Dar Meshi,et al.  Eye movements reset visual perception. , 2012, Journal of vision.

[30]  F. Qiu,et al.  Figure and Ground in the Visual Cortex: V2 Combines Stereoscopic Cues with Gestalt Rules , 2005, Neuron.

[31]  R. Kötter,et al.  Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits , 2007, Brain Structure and Function.

[32]  Timothée Masquelier,et al.  Unsupervised Learning of Visual Features through Spike Timing Dependent Plasticity , 2007, PLoS Comput. Biol..

[33]  Shawn R. Olsen,et al.  Gain control by layer six in cortical circuits of vision , 2012, Nature.

[34]  Gayle M. Wittenberg,et al.  Spike Timing Dependent Plasticity: A Consequence of More Fundamental Learning Rules , 2010, Front. Comput. Neurosci..

[35]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[36]  S. Shimojo,et al.  Visual illusion induced by sound. , 2002, Brain research. Cognitive brain research.

[37]  G. Avanzini,et al.  Ionic mechanisms underlying burst firing in pyramidal neurons: intracellular study in rat sensorimotor cortex , 1995, Brain Research.

[38]  C. Summerfield,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008, Nature Neuroscience.

[39]  K. Mathewson,et al.  Rescuing stimuli from invisibility: Inducing a momentary release from visual masking with pre-target entrainment , 2010, Cognition.

[40]  David A. Leopold,et al.  Distinct Superficial and Deep Laminar Domains of Activity in the Visual Cortex during Rest and Stimulation , 2010, Front. Syst. Neurosci..

[41]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[42]  David J. Jilk,et al.  Recurrent Processing during Object Recognition , 2011, Front. Psychol..

[43]  C. Koch,et al.  The continuous wagon wheel illusion is associated with changes in electroencephalogram power at approximately 13 Hz. , 2006, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  R. VanRullen,et al.  An oscillatory mechanism for prioritizing salient unattended stimuli , 2012, Trends in Cognitive Sciences.

[45]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[46]  P. Fries,et al.  Attention Samples Stimuli Rhythmically , 2012, Current Biology.

[47]  Stephen Grossberg,et al.  A massively parallel architecture for a self-organizing neural pattern recognition machine , 1988, Comput. Vis. Graph. Image Process..

[48]  J. Elman Distributed representations, simple recurrent networks, and grammatical structure , 1991, Machine Learning.

[49]  Alex M. Thomson,et al.  Neocortical Layer 6, A Review , 2010, Front. Neuroanat..

[50]  Pascal Vincent,et al.  Representation Learning: A Review and New Perspectives , 2012, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[51]  G. Karmos,et al.  Transient cortical excitation at the onset of visual fixation. , 2008, Cerebral cortex.

[52]  Garrison W. Cottrell,et al.  Organization of face and object recognition in modular neural network models , 1999, Neural Networks.

[53]  D. Spalding The Principles of Psychology , 1873, Nature.

[54]  Sebastian Müller,et al.  Alpha entrainment is responsible for the attentional blink phenomenon , 2012, NeuroImage.

[55]  Sonja Grün,et al.  Saccade-Related Modulations of Neuronal Excitability Support Synchrony of Visually Elicited Spikes , 2011, Cerebral cortex.

[56]  R A Young,et al.  The Gaussian derivative model for spatial vision: I. Retinal mechanisms. , 1988, Spatial vision.

[57]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[58]  Wulfram Gerstner,et al.  Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. , 2005, Journal of neurophysiology.

[59]  Randall C. O'Reilly,et al.  Generalization in Interactive Networks: The Benefits of Inhibitory Competition and Hebbian Learning , 2001, Neural Computation.

[60]  Axel Cleeremans,et al.  Mechanisms of Implicit Learning: Connectionist Models of Sequence Processing , 1993 .

[61]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[62]  Jordan B. Pollack,et al.  Recursive Distributed Representations , 1990, Artif. Intell..

[63]  Corinna Cortes,et al.  Support-Vector Networks , 1995, Machine Learning.

[64]  E. Newport,et al.  Computation of Conditional Probability Statistics by 8-Month-Old Infants , 1998 .

[65]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[66]  D. Mumford,et al.  Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency , 2002, Nature Neuroscience.

[67]  G. Kane Parallel Distributed Processing: Explorations in the Microstructure of Cognition, vol 1: Foundations, vol 2: Psychological and Biological Models , 1994 .

[68]  S. Murray Sherman,et al.  Modulator Property of the Intrinsic Cortical Projection from Layer 6 to Layer 4 , 2009, Front. Syst. Neurosci..

[69]  F. Castellanos,et al.  Entrainment of neural oscillations as a modifiable substrate of attention , 2014, Trends in Cognitive Sciences.

[70]  James L. McClelland,et al.  Finite State Automata and Simple Recurrent Networks , 1989, Neural Computation.

[71]  Geoffrey E. Hinton,et al.  A Learning Algorithm for Boltzmann Machines , 1985, Cogn. Sci..

[72]  B. Connors,et al.  Two types of network oscillations in neocortex mediated by distinct glutamate receptor subtypes and neuronal populations. , 1996, Journal of neurophysiology.

[73]  Alexander Maier,et al.  Infragranular Sources of Sustained Local Field Potential Responses in Macaque Primary Visual Cortex , 2011, The Journal of Neuroscience.

[74]  Geoffrey E. Hinton,et al.  Discovering High Order Features with Mean Field Modules , 1989, NIPS.

[75]  Yoshua Bengio,et al.  Greedy Layer-Wise Training of Deep Networks , 2006, NIPS.

[76]  D. Leopold,et al.  Layer-Specific Entrainment of Gamma-Band Neural Activity by the Alpha Rhythm in Monkey Visual Cortex , 2012, Current Biology.

[77]  Wulfram Gerstner,et al.  How Good Are Neuron Models? , 2009, Science.

[78]  Alejandro Lleras,et al.  Making Waves in the Stream of Consciousness: Entraining Oscillations in EEG Alpha and Fluctuations in Visual Awareness with Rhythmic Visual Stimulation , 2012, Journal of Cognitive Neuroscience.

[79]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[80]  Randall C. O'Reilly,et al.  Biologically Plausible Error-Driven Learning Using Local Activation Differences: The Generalized Recirculation Algorithm , 1996, Neural Computation.

[81]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[82]  C. Koch,et al.  The Continuous Wagon Wheel Illusion Is Associated with Changes in Electroencephalogram Power at ∼13 Hz , 2006, The Journal of Neuroscience.

[83]  R. von der Heydt,et al.  A neural model of figure-ground organization. , 2007, Journal of neurophysiology.

[84]  Mark H. Johnson,et al.  Dynamic Plasticity Influences the Emergence of Function in a Simple Cortical Array , 1996, Neural Networks.

[85]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[86]  Geoffrey E. Hinton,et al.  Learning Representations by Recirculation , 1987, NIPS.

[87]  S. Hughes,et al.  Temporal Framing of Thalamic Relay-Mode Firing by Phasic Inhibition during the Alpha Rhythm , 2009, Neuron.

[88]  James L. McClelland,et al.  Parallel distributed processing: explorations in the microstructure of cognition, vol. 1: foundations , 1986 .

[89]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[90]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[91]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[92]  R. Granger,et al.  Derivation and Analysis of Basic Computational Operations of Thalamocortical Circuits , 2004, Journal of Cognitive Neuroscience.

[93]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[94]  Judith A Hirsch,et al.  Laminar processing in the visual cortical column , 2006, Current Opinion in Neurobiology.

[95]  A. Thomson,et al.  Functional Maps of Neocortical Local Circuitry , 2007, Front. Neurosci..

[96]  H. Urakubo,et al.  Requirement of an Allosteric Kinetics of NMDA Receptors for Spike Timing-Dependent Plasticity , 2008, The Journal of Neuroscience.

[97]  Caspar M. Schwiedrzik,et al.  (Micro)Saccades, corollary activity and cortical oscillations , 2009, Trends in Cognitive Sciences.

[98]  Jeffrey L. Elman,et al.  Finding Structure in Time , 1990, Cogn. Sci..

[99]  K. Harris,et al.  Gating of Sensory Input by Spontaneous Cortical Activity , 2013, The Journal of Neuroscience.

[100]  Luca Maria Gambardella,et al.  Deep, Big, Simple Neural Nets for Handwritten Digit Recognition , 2010, Neural Computation.

[101]  Geoffrey E. Hinton,et al.  Learning representations by back-propagating errors , 1986, Nature.

[102]  Rufin VanRullen,et al.  The Flickering Wheel Illusion: When α Rhythms Make a Static Wheel Flicker , 2013, The Journal of Neuroscience.

[103]  Li Zhaoping,et al.  Border Ownership from Intracortical Interactions in Visual Area V2 , 2005, Neuron.

[104]  Jürgen Schmidhuber,et al.  Multi-column deep neural networks for image classification , 2012, 2012 IEEE Conference on Computer Vision and Pattern Recognition.

[105]  John J. Foxe,et al.  Ready, Set, Reset: Stimulus-Locked Periodicity in Behavioral Performance Demonstrates the Consequences of Cross-Sensory Phase Reset , 2011, The Journal of Neuroscience.

[106]  Maarten De Vos,et al.  Endogenous and Rapid Serial Visual Presentation-induced Alpha Band Oscillations in the Attentional Blink , 2014, Journal of Cognitive Neuroscience.

[107]  Dileep George,et al.  Towards a Mathematical Theory of Cortical Micro-circuits , 2009, PLoS Comput. Biol..

[108]  E. Spaak,et al.  Local Entrainment of Alpha Oscillations by Visual Stimuli Causes Cyclic Modulation of Perception , 2014, The Journal of Neuroscience.

[109]  Jean Bullier,et al.  The Timing of Information Transfer in the Visual System , 1997 .

[110]  E. John,et al.  Perceptual framing and cortical alpha rhythm , 1981, Neuropsychologia.

[111]  B. Connors,et al.  Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. , 1991, Science.

[112]  J. Elman,et al.  Rethinking Innateness: A Connectionist Perspective on Development , 1996 .

[113]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[114]  W. Singer,et al.  Synchronization of neuronal responses in primary visual cortex of monkeys viewing natural images. , 2008, Journal of neurophysiology.

[115]  C. Koch,et al.  Attention-driven discrete sampling of motion perception. , 2005, Proceedings of the National Academy of Sciences of the United States of America.