A Three-Threshold Learning Rule Approaches the Maximal Capacity of Recurrent Neural Networks

Understanding the theoretical foundations of how memories are encoded and retrieved in neural populations is a central challenge in neuroscience. A popular theoretical scenario for modeling memory function is the attractor neural network scenario, whose prototype is the Hopfield model. The model simplicity and the locality of the synaptic update rules come at the cost of a poor storage capacity, compared with the capacity achieved with perceptron learning algorithms. Here, by transforming the perceptron learning rule, we present an online learning rule for a recurrent neural network that achieves near-maximal storage capacity without an explicit supervisory error signal, relying only upon locally accessible information. The fully-connected network consists of excitatory binary neurons with plastic recurrent connections and non-plastic inhibitory feedback stabilizing the network dynamics; the memory patterns to be memorized are presented online as strong afferent currents, producing a bimodal distribution for the neuron synaptic inputs. Synapses corresponding to active inputs are modified as a function of the value of the local fields with respect to three thresholds. Above the highest threshold, and below the lowest threshold, no plasticity occurs. In between these two thresholds, potentiation/depression occurs when the local field is above/below an intermediate threshold. We simulated and analyzed a network of binary neurons implementing this rule and measured its storage capacity for different sizes of the basins of attraction. The storage capacity obtained through numerical simulations is shown to be close to the value predicted by analytical calculations. We also measured the dependence of capacity on the strength of external inputs. Finally, we quantified the statistics of the resulting synaptic connectivity matrix, and found that both the fraction of zero weight synapses and the degree of symmetry of the weight matrix increase with the number of stored patterns.

[1]  A. A. Mullin,et al.  Principles of neurodynamics , 1962 .

[2]  J. Buhmann,et al.  Associative memory with high information content. , 1989, Physical review. A, General physics.

[3]  Nicolas Brunel,et al.  Lapicque’s 1907 paper: from frogs to integrate-and-fire , 2007, Biological Cybernetics.

[4]  Yali Amit,et al.  Attractor Networks for Shape Recognition , 2001, Neural Computation.

[5]  Walter Senn,et al.  Learning Real-World Stimuli in a Neural Network with Spike-Driven Synaptic Dynamics , 2007, Neural Computation.

[6]  Tatsuya Uezu,et al.  The Phase Space of Interactions and the Hebb Rule in the Neural Network Models , 1996 .

[7]  Masao Ito,et al.  Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells , 1982, The Journal of physiology.

[8]  Sompolinsky,et al.  Neural networks with nonlinear synapses and a static noise. , 1986, Physical review. A, General physics.

[9]  Y. Miyashita,et al.  Neuronal correlate of pictorial short-term memory in the primate temporal cortexYasushi Miyashita , 1988, Nature.

[10]  Anders Krogh,et al.  Introduction to the theory of neural computation , 1994, The advanced book program.

[11]  J. Nadal,et al.  What can we learn from synaptic weight distributions? , 2007, Trends in Neurosciences.

[12]  A. Artola,et al.  Synaptic Activity Modulates the Induction of Bidirectional Synaptic Changes in Adult Mouse Hippocampus , 2000, The Journal of Neuroscience.

[13]  J. Nadal,et al.  Optimal Information Storage and the Distribution of Synaptic Weights Perceptron versus Purkinje Cell , 2004, Neuron.

[14]  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.

[15]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[16]  Marc Mézard,et al.  Solvable models of working memories , 1986 .

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

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

[19]  W Singer,et al.  Intracellular injection of Ca2+ chelators blocks induction of long-term depression in rat visual cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Nicolas Brunel,et al.  Storage of Correlated Patterns in Standard and Bistable Purkinje Cell Models , 2012, PLoS Comput. Biol..

[21]  K. Nakamura,et al.  Mnemonic firing of neurons in the monkey temporal pole during a visual recognition memory task. , 1995, Journal of neurophysiology.

[22]  M. Tsodyks,et al.  Working models of working memory , 2014, Current Opinion in Neurobiology.

[23]  M. Tsodyks,et al.  The Enhanced Storage Capacity in Neural Networks with Low Activity Level , 1988 .

[24]  E. Gardner,et al.  An Exactly Solvable Asymmetric Neural Network Model , 1987 .

[25]  H Wang,et al.  Priming-induced shift in synaptic plasticity in the rat hippocampus. , 1999, Journal of neurophysiology.

[26]  W S McCulloch,et al.  A logical calculus of the ideas immanent in nervous activity , 1990, The Philosophy of Artificial Intelligence.

[27]  J. Albus A Theory of Cerebellar Function , 1971 .

[28]  H. Markram,et al.  The neocortical microcircuit as a tabula rasa. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  G. Parisi A memory which forgets , 1986 .

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

[31]  G. Parisi,et al.  Asymmetric neural networks and the process of learning , 1986 .

[32]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[33]  Sompolinsky,et al.  Storing infinite numbers of patterns in a spin-glass model of neural networks. , 1985, Physical review letters.

[34]  Julio Chapeton,et al.  Efficient associative memory storage in cortical circuits of inhibitory and excitatory neurons , 2012, Proceedings of the National Academy of Sciences.

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

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

[37]  W. Singer,et al.  Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation , 1993, Trends in Neurosciences.

[38]  P. Jedlicka,et al.  Synaptic plasticity, metaplasticity and BCM theory. , 2002, Bratislavske lekarske listy.

[39]  John J. Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities , 1999 .

[40]  N Brunel,et al.  Slow stochastic Hebbian learning of classes of stimuli in a recurrent neural network. , 1998, Network.

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

[42]  Xiao-Jing Wang,et al.  Erratum to: Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition , 2014, Journal of Computational Neuroscience.

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

[44]  M. Bear,et al.  Experience-dependent modification of synaptic plasticity in visual cortex , 1996, Nature.

[45]  L. Abbott,et al.  Cascade Models of Synaptically Stored Memories , 2005, Neuron.

[46]  Thomas K. Berger,et al.  Heterogeneity in the pyramidal network of the medial prefrontal cortex , 2006, Nature Neuroscience.

[47]  E. Gardner The space of interactions in neural network models , 1988 .

[48]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[49]  Daniel J. Amit,et al.  Learning in Neural Networks with Material Synapses , 1994, Neural Computation.

[50]  Nicolas Brunel,et al.  Optimal Properties of Analog Perceptrons with Excitatory Weights , 2013, PLoS Comput. Biol..

[51]  Néstor Parga,et al.  The ultrametric organization of memories in a neural network , 1986 .

[52]  N. Stanietsky,et al.  The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity , 2009, Proceedings of the National Academy of Sciences.

[53]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.