Comparison of computational models of familiarity discrimination in the perirhinal cortex

This study compares the efficiency and plausibility of published computational models of familiarity discrimination in the perirhinal cortex. Substantial evidence indicates that the perirhinal cortex is involved in both the familiarity discrimination aspect of recognition memory and in perceptual functions involved with representations of complete stimuli (i.e., object identification). Published models of how the perirhinal cortex may perform familiarity discrimination can be divided into two groups. The first group assumes that a proportion of perirhinal neurons form a network specialised just for familiarity discrimination (these models may be based on Hebbian or anti‐Hebbian synaptic plasticity). In contrast, the second group assumes that both familiarity discrimination and learning representations of complete stimuli are performed within a single combined network. This study establishes that when the responses of neurons that provide input to the familiarity discrimination network are correlated (as indicated by experimental data), specialised networks based on anti‐Hebbian learning may recognise the previous occurrence of many more stimuli (i.e., have a capacity up to thousands of times larger) than specialised networks based on Hebbian learning. The currently published combined models do not learn an optimal stimulus representation (they do not fully extract statistically independent features), and hence their capacities are even lower than those of the specialised models based on Hebbian learning. Hence, the combined models published thus far are critically less efficient than the specialised models based on anti‐Hebbian learning. This study also compares the consistency of the models with experimental observations concerning what is known of synaptic plasticity in the perirhinal cortex and the responses of its neurons. Many theoretically important parameters remain undetermined, and experiments are suggested to provide information critical for refining and distinguishing between the various models. However, the above theoretical arguments and currently published data favour the existence of a separate network specialised for familiarity discrimination. Hippocampus 2003;13:494–524. © 2003 Wiley‐Liss, Inc.

[1]  J. Ringo,et al.  Stimulus specific adaptation in excited but not in inhibited cells in inferotemporal cortex of Macaque , 1994, Brain Research.

[2]  W. Suzuki,et al.  Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[4]  Keiji Tanaka,et al.  Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. , 1998, Journal of neurophysiology.

[5]  M W Brown,et al.  Differential neuronal responsiveness in primate perirhinal cortex and hippocampal formation during performance of a conditional visual discrimination task , 1999, The European journal of neuroscience.

[6]  Rafal Bogacz,et al.  Frequency-based error backpropagation in a cortical network , 2000, Proceedings of the IEEE-INNS-ENNS International Joint Conference on Neural Networks. IJCNN 2000. Neural Computing: New Challenges and Perspectives for the New Millennium.

[7]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[8]  Wulfram Gerstner,et al.  Spontaneous Excitations in the Visual Cortex: Stripes, Spirals, Rings, and Collective Bursts , 1995, Neural Computation.

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

[10]  Lucas C. Parra,et al.  Statistical Independence and Novelty Detection with Information Preserving Nonlinear Maps , 1996, Neural Computation.

[11]  A. Sharkey,et al.  The septo-hippocampal system and anxiety: a robot simulation , 1999 .

[12]  D. Mumby,et al.  Rhinal cortex lesions and object recognition in rats. , 1994, Behavioral neuroscience.

[13]  P S Goldman-Rakic,et al.  Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Wolfgang Maass,et al.  Spiking Neurons , 1998, NC.

[15]  S. Nelson,et al.  Hebb and homeostasis in neuronal plasticity , 2000, Current Opinion in Neurobiology.

[16]  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.

[17]  M. Mishkin,et al.  Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[19]  H. B. Barlow,et al.  Unsupervised Learning , 1989, Neural Computation.

[20]  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.

[21]  Z. Bashir,et al.  Long-term depression: a cascade of induction and expression mechanisms , 2001, Progress in Neurobiology.

[22]  Stephen J. Roberts,et al.  A Probabilistic Resource Allocating Network for Novelty Detection , 1994, Neural Computation.

[23]  Rafal Bogacz,et al.  The restricted influence of sparseness of coding on the capacity of familiarity discrimination networks , 2002, Network.

[24]  J. Aggleton,et al.  Amnesia and recognition memory: A re-analysis of psychometric data , 1996, Neuropsychologia.

[25]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[26]  M W Brown,et al.  GABAB receptors mediate frequency‐dependent depression of excitatory potentials in rat perirhinal cortex in vitro , 2000, The European journal of neuroscience.

[27]  M. Dragunow A role for immediate-early transcription factors in learning and memory , 1996, Behavior genetics.

[28]  C. Blackstone The Neuron: Cell and Molecular Biology , 2003 .

[29]  Niraj S. Desai,et al.  Activity-dependent scaling of quantal amplitude in neocortical neurons , 1998, Nature.

[30]  H. Soininen,et al.  MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. , 1998, AJNR. American journal of neuroradiology.

[31]  P. Dayan,et al.  Optimising synaptic learning rules in linear associative memories , 1991, Biological Cybernetics.

[32]  P. C. M. F. J. Owens BSc Signal Processing of Speech , 1993, Macmillan New Electronics Series.

[33]  B. McNaughton,et al.  Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. , 1990, Progress in brain research.

[34]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  Malcolm W. Brown,et al.  Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory , 1999, The Journal of Neuroscience.

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

[37]  GrossbergS. Adaptive pattern classification and universal recoding , 1976 .

[38]  E. J. Rowe,et al.  Continuous judgments of word frequency and familiarity. , 1972 .

[39]  Niraj S. Desai,et al.  Plasticity in the intrinsic excitability of cortical pyramidal neurons , 1999, Nature Neuroscience.

[40]  R. Burwell The Parahippocampal Region: Corticocortical Connectivity , 2000, Annals of the New York Academy of Sciences.

[41]  TJ Gawne,et al.  How independent are the messages carried by adjacent inferior temporal cortical neurons? , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Rajesh P. N. Rao,et al.  Efficient Encoding of Natural Time Varying Images Produces Oriented Space-Time Receptive Fields , 1997 .

[43]  R W Prager,et al.  Development of low entropy coding in a recurrent network. , 1996, Network.

[44]  C. Malsburg Self-organization of orientation sensitive cells in the striate cortex , 2004, Kybernetik.

[45]  S. Grossberg,et al.  Adaptive pattern classification and universal recoding: I. Parallel development and coding of neural feature detectors , 1976, Biological Cybernetics.

[46]  T. H. Brown,et al.  Morphology and physiology of neurons in the rat perirhinal‐lateral amygdala area , 1999, The Journal of comparative neurology.

[47]  Michael J. Berry,et al.  The Neural Code of the Retina , 1999, Neuron.

[48]  J L Ringo Brevity of processing in a mnemonic task. , 1995, Journal of neurophysiology.

[49]  Colin Campbell,et al.  A Linear Programming Approach to Novelty Detection , 2000, NIPS.

[50]  James L. McClelland,et al.  A Hippocampal Model of Recognition Memory , 1997, NIPS.

[51]  R. Desimone,et al.  Scopolamine affects short-term memory but not inferior temporal neurons. , 1993, Neuroreport.

[52]  D. Manahan‐Vaughan,et al.  Novelty acquisition is associated with induction of hippocampal long-term depression. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[53]  D. Bilkey,et al.  Synchronous modulation of perirhinal cortex neuronal activity during cholinergically mediated (type II) hippocampal theta , 1998, Hippocampus.

[54]  David J. Field,et al.  Sparse coding with an overcomplete basis set: A strategy employed by V1? , 1997, Vision Research.

[55]  I. Riches,et al.  The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  Terrence J. Sejnowski,et al.  Unsupervised Learning , 2018, Encyclopedia of GIS.

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

[58]  David J. Field,et al.  Emergence of simple-cell receptive field properties by learning a sparse code for natural images , 1996, Nature.

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

[60]  David A. Caulton,et al.  Retrieval dynamics in recognition and list discrimination: Further evidence of separate processes of familiarity and recall , 1998, Memory & cognition.

[61]  M W Brown,et al.  Mapping visual recognition memory through expression of the immediate early gene c-fos. , 1996, Neuroreport.

[62]  D. Hubel,et al.  Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. , 1965, Journal of neurophysiology.

[63]  Aapo Hyvärinen,et al.  Sparse Code Shrinkage: Denoising of Nongaussian Data by Maximum Likelihood Estimation , 1999, Neural Computation.

[64]  Daniel L. Schacter,et al.  When True Recognition Suppresses False Recognition: Evidence from Amnesic Patients , 1998, Journal of Cognitive Neuroscience.

[65]  Wulfram Gerstner Populations of spiking neurons , 1999 .

[66]  Peter Dayan,et al.  Optimal Plasticity from Matrix Memories: What Goes Up Must Come Down , 1990, Neural Computation.

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

[68]  E. Halgren,et al.  Anatomical origin of déjà vu and vivid 'memories' in human temporal lobe epilepsy. , 1994, Brain : a journal of neurology.

[69]  L. Squire,et al.  The human perirhinal cortex and recognition memory , 1998, Hippocampus.

[70]  I. Fujita,et al.  Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex , 2000, Nature Neuroscience.

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

[72]  Bruno A. Olshausen,et al.  Sparse Coding Of Time-Varying Natural Images , 2010 .

[73]  R. Palmer,et al.  , Introduction to the Theory of Neural Computation 1 , 2007 .

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

[75]  T. Albright,et al.  Efficient Discrimination of Temporal Patterns by Motion-Sensitive Neurons in Primate Visual Cortex , 1998, Neuron.

[76]  Stephen Grossberg,et al.  Familiarity Discrimination of Radar Pulses , 1998, NIPS.

[77]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

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

[79]  C L Baker,et al.  Spatial- and temporal-frequency selectivity as a basis for velocity preference in cat striate cortex neurons , 1990, Visual Neuroscience.

[80]  D. Ruderman,et al.  Independent component analysis of natural image sequences yields spatio-temporal filters similar to simple cells in primary visual cortex , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[81]  Y. Prigent [Long term depression]. , 1989, Annales medico-psychologiques.

[82]  M. Segal Rapid plasticity of dendritic spine: hints to possible functions? , 2001, Progress in Neurobiology.

[83]  David Willshaw,et al.  Models of distributed associative memory , 1971 .

[84]  E. Rolls A theory of hippocampal function in memory , 1996, Hippocampus.

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

[86]  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.

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

[88]  D. Schacter The seven sins of memory. Insights from psychology and cognitive neuroscience. , 1999, The American psychologist.

[89]  P. Fiildihk,et al.  Forming sparse representations by local anti-Hebbian learning , 1990 .

[90]  F. H. Lopes da Silva,et al.  Cortico‐hippocampal communication by way of parallel parahippocampal‐subicular pathways , 2000, Hippocampus.

[91]  Ramez Elmasri,et al.  Fundamentals of Database Systems , 1989 .

[92]  K. Harris,et al.  Slices Have More Synapses than Perfusion-Fixed Hippocampus from both Young and Mature Rats , 1999, The Journal of Neuroscience.

[93]  D. Amaral,et al.  Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  M. Hasselmo,et al.  A model for experience-dependent changes in the responses of inferotemporal neurons , 2000, Network.

[95]  T. Bussey,et al.  Perceptual–mnemonic functions of the perirhinal cortex , 1999, Trends in Cognitive Sciences.

[96]  Christopher M. Bishop,et al.  Novelty detection and neural network validation , 1994 .

[97]  R. Palmer,et al.  Introduction to the theory of neural computation , 1994, The advanced book program.

[98]  M. Tovée,et al.  Processing speed in the cerebral cortex and the neurophysiology of visual masking , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[99]  M. W. Brown,et al.  A new form of long-term depression in the perirhinal cortex , 2000, Nature Neuroscience.

[100]  E. K. Miller,et al.  Functional interactions among neurons in inferior temporal cortex of the awake macaque , 2004, Experimental Brain Research.

[101]  H. Mitoma,et al.  Monoaminergic long-term facilitation of GABA-mediated inhibitory transmission at cerebellar synapses , 1999, Neuroscience.

[102]  D. Gaffan,et al.  Perirhinal Cortex Ablation Impairs Visual Object Identification , 1998, The Journal of Neuroscience.

[103]  Kari Torkkola,et al.  Blind separation of convolved sources based on information maximization , 1996, Neural Networks for Signal Processing VI. Proceedings of the 1996 IEEE Signal Processing Society Workshop.

[104]  Terrence J. Sejnowski,et al.  Edges are the Independent Components of Natural Scenes , 1996, NIPS.

[105]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[106]  Rafal Bogacz,et al.  Emergence of Movement Sensitive Neurons' Properties by Learning a Sparse Code for Natural Moving Images , 2000, NIPS.

[107]  R. Desimone,et al.  Clustering of perirhinal neurons with similar properties following visual experience in adult monkeys , 2000, Nature Neuroscience.

[108]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[109]  M. Hasselmo,et al.  The effect of learning on the face selective responses of neurons in the cortex in the superior temporal sulcus of the monkey , 2004, Experimental Brain Research.

[110]  Teuvo Kohonen,et al.  Self-Organization and Associative Memory , 1988 .

[111]  David Willshaw,et al.  Capacity and information efficiency of the associative net , 1997 .

[112]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[113]  K M Harris,et al.  Stability in Synapse Number and Size at 2 Hr after Long-Term Potentiation in Hippocampal Area CA1 , 1998, The Journal of Neuroscience.

[114]  Rafal Bogacz,et al.  Model of co-operation between recency, familiarity and novelty neurons in the perirhinal cortex , 2001, Neurocomputing.

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

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

[117]  Christophe Giraud-Carrier,et al.  High Capacity Neural Networks for Familiarity Discrimination , 1999 .

[118]  Elisabeth A. Murray,et al.  What have ablation studies told us about the neural substrates of stimulus memory , 1996 .

[119]  Christopher J. Bishop,et al.  Pulsed Neural Networks , 1998 .

[120]  C. Koch,et al.  Category-specific visual responses of single neurons in the human medial temporal lobe , 2000, Nature Neuroscience.

[121]  D. Bilkey Long-term potentiation in the in vitro perirhinal cortex displays associative properties , 1996, Brain Research.

[122]  D. Marr A theory for cerebral neocortex , 1970, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[123]  Günther Palm,et al.  Information capacity in recurrent McCulloch-Pitts networks with sparsely coded memory states , 1992 .

[124]  A. Hodgkin,et al.  The frequency of nerve action potentials generated by applied currents , 1967, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[125]  Leon N. Cooper,et al.  Formation of Direction Selectivity in Natural Scene Environments , 2000, Neural Computation.

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

[127]  Erkki Oja,et al.  Adaptation of a linear system to a finite set of patterns occurring in an arbitrarily varying order , 1974 .

[128]  Wendy A Suzuki,et al.  The anatomy, physiology and functions of the perirhinal cortex , 1996, Current Opinion in Neurobiology.

[129]  DH Hubel,et al.  Psychophysical evidence for separate channels for the perception of form, color, movement, and depth , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[130]  W. A. Wilson,et al.  GABAB autoreceptors mediate activity-dependent disinhibition and enhance signal transmission in the dentate gyrus. , 1993, Journal of neurophysiology.

[131]  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.

[132]  H. Markram,et al.  Redistribution of synaptic efficacy between neocortical pyramidal neurons , 1996, Nature.

[133]  M. W. Brown,et al.  Input- and layer-dependent synaptic plasticity in the rat perirhinal cortex in vitro , 1999, Neuroscience.

[134]  C. Michel,et al.  Evidence for rapid face recognition from human scalp and intracranial electrodes , 1997, Neuroreport.

[135]  Adam Kowalczyk,et al.  Estimates of Storage Capacity of Multilayer Perceptron with Threshold Logic Hidden Units , 1997, Neural Networks.

[136]  E. Murray,et al.  Impairments in visual discrimination learning and recognition memory produced by neurotoxic lesions of rhinal cortex in rhesus monkeys , 2001, The European journal of neuroscience.

[137]  W. Pitts,et al.  A Logical Calculus of the Ideas Immanent in Nervous Activity (1943) , 2021, Ideas That Created the Future.

[138]  Rafal Bogacz,et al.  A Familiarity Discrimination Algorithm Inspired by Computations of the Perirhinal Cortex , 2001, Emergent Neural Computational Architectures Based on Neuroscience.