Universal Memory Mechanism for Familiarity Recognition and Identification

Macaque monkeys were tested on a delayed-match-to-multiple-sample task, with either a limited set of well trained images (in randomized sequence) or with never-before-seen images. They performed much better with novel images. False positives were mostly limited to catch-trial image repetitions from the preceding trial. This result implies extremely effective one-shot learning, resembling Standing's finding that people detect familiarity for 10,000 once-seen pictures (with 80% accuracy) (Standing, 1973). Familiarity memory may differ essentially from identification, which embeds and generates contextual information. When encountering another person, we can say immediately whether his or her face is familiar. However, it may be difficult for us to identify the same person. To accompany the psychophysical findings, we present a generic neural network model reproducing these behaviors, based on the same conservative Hebbian synaptic plasticity that generates delay activity identification memory. Familiarity becomes the first step toward establishing identification. Adding an inter-trial reset mechanism limits false positives for previous-trial images. The model, unlike previous proposals, relates repetition–recognition with enhanced neural activity, as recently observed experimentally in 92% of differential cells in prefrontal cortex, an area directly involved in familiarity recognition. There may be an essential functional difference between enhanced responses to novel versus to familiar images: The maximal signal from temporal cortex is for novel stimuli, facilitating additional sensory processing of newly acquired stimuli. The maximal signal for familiar stimuli arising in prefrontal cortex facilitates the formation of selective delay activity, as well as additional consolidation of the memory of the image in an upstream cortical module.

[1]  Walter L. Smith Probability and Statistics , 1959, Nature.

[2]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

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

[4]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[5]  L. Standing Learning 10000 pictures , 1973 .

[6]  L. Standing Learning 10,000 pictures. , 1973, The Quarterly journal of experimental psychology.

[7]  Richard Passingham,et al.  Delayed matching after selective prefrontal lesions in monkeys (Macaca mulatta) , 1975, Brain Research.

[8]  J. Fuster,et al.  Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys. , 1976, Journal of comparative and physiological psychology.

[9]  M. Mishkin,et al.  Non-spatial memory after selective prefrontal lesions in monkeys , 1978, Brain Research.

[10]  G. Mandler Recognizing: The judgment of previous occurrence. , 1980 .

[11]  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.

[12]  Stanislas Dehaene,et al.  Networks of Formal Neurons and Memory Palimpsests , 1986 .

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

[14]  M. W. Brown,et al.  Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory , 1987, Brain Research.

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

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

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

[18]  M. Tsodyks ASSOCIATIVE MEMORY IN NEURAL NETWORKS WITH BINARY SYNAPSES , 1990 .

[19]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[20]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

[21]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  Y. Miyashita Inferior temporal cortex: where visual perception meets memory. , 1993, Annual review of neuroscience.

[23]  R. Desimone,et al.  The representation of stimulus familiarity in anterior inferior temporal cortex. , 1993, Journal of neurophysiology.

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

[25]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[26]  N Brunel,et al.  Correlations of cortical Hebbian reverberations: theory versus experiment , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  D. Amit The Hebbian paradigm reintegrated: Local reverberations as internal representations , 1995, Behavioral and Brain Sciences.

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

[29]  L. Abbott,et al.  A model of multiplicative neural responses in parietal cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

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

[32]  J. Hopfield,et al.  All-or-none potentiation at CA3-CA1 synapses. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[34]  M. W. Brown,et al.  Recognition memory: neuronal substrates of the judgement of prior occurrence , 1998, Progress in Neurobiology.

[35]  Daniel J. Amit,et al.  Simulation in neurobiology: theory or experiment? , 1998, Trends in Neurosciences.

[36]  E. Miller,et al.  Neural Activity in the Primate Prefrontal Cortex during Associative Learning , 1998, Neuron.

[37]  M. W. Brown,et al.  Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe , 1998, Neuropharmacology.

[38]  R. Desimone,et al.  Responses of Macaque Perirhinal Neurons during and after Visual Stimulus Association Learning , 1999, The Journal of Neuroscience.

[39]  Davide Badoni,et al.  Spike-Driven Synaptic Plasticity: Theory, Simulation, VLSI Implementation , 2000, Neural Computation.

[40]  J. D. McGaugh Memory--a century of consolidation. , 2000, Science.

[41]  Malcolm W. Brown,et al.  Recognition memory: What are the roles of the perirhinal cortex and hippocampus? , 2001, Nature Reviews Neuroscience.

[42]  Edmund T. Rolls,et al.  Perirhinal Cortex Neuronal Activity is Actively Related to Working Memory in the Macaque , 2002, Neural plasticity.

[43]  Rafal Bogacz,et al.  Comparison of computational models of familiarity discrimination in the perirhinal cortex , 2003, Hippocampus.

[44]  D. Amit,et al.  Retrospective and prospective persistent activity induced by Hebbian learning in a recurrent cortical network , 2003, The European journal of neuroscience.

[45]  Daniel J. Amit,et al.  Spike-Driven Synaptic Dynamics Generating Working Memory States , 2003, Neural Computation.

[46]  D J Amit,et al.  Multiple-object working memory--a model for behavioral performance. , 2003, Cerebral cortex.

[47]  R. O’Reilly,et al.  Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. , 2003, Psychological review.

[48]  M. W. Brown,et al.  Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex , 2004, Experimental Brain Research.

[49]  Malcolm W. Brown,et al.  Neuronal Responses Related to Long-Term Recognition Memory Processes in Prefrontal Cortex , 2004, Neuron.

[50]  J. Ringo,et al.  Investigation of long term recognition and association memory in unit responses from inferotemporal cortex , 1993, Experimental Brain Research.

[51]  Xiao-Jing Wang,et al.  A Model of Visuospatial Working Memory in Prefrontal Cortex: Recurrent Network and Cellular Bistability , 1998, Journal of Computational Neuroscience.

[52]  Rafal Bogacz,et al.  Model of Familiarity Discrimination in the Perirhinal Cortex , 2004, Journal of Computational Neuroscience.

[53]  D. Gaffan,et al.  Impaired Recency Judgments and Intact Novelty Judgments after Fornix Transection in Monkeys , 2004, Journal of Neuroscience.

[54]  Shaul Hochstein,et al.  Multi-item working memory--a behavioral study. , 2005, Cerebral cortex.

[55]  M. Gluck,et al.  Integrating incremental learning and episodic memory models of the hippocampal region. , 2005, Psychological review.

[56]  Sandro Romani,et al.  Learning in realistic networks of spiking neurons and spike‐driven plastic synapses , 2005, The European journal of neuroscience.