The Perirhinal Cortex and Long-Term Familiarity Memory

To analyse the functions of the perirhinal cortex, the activity of single neurons in the perirhinal cortex was recorded while macaques performed a delayed matching-to-sample task with up to three intervening stimuli. Some neurons had activity related to working memory, in that they responded more to the sample than to the match image within a trial, as shown previously. However, when a novel set of stimuli was introduced, the neuronal responses were on average only 47% of the magnitude of the responses to the set of very familiar stimuli. Moreover, it was shown in three monkeys that the responses of the perirhinal cortex neurons gradually increased over hundreds of presentations (mean = 400 over 7–13 days) of the new set of (initially novel) stimuli to become as large as those to the already familiar stimuli. Thus perirhinal cortex neurons represent the very long-term familiarity of visual stimuli. Part of the impairment in temporal lobe amnesia may be related to the difficulty of building representations of the degree of familiarity of stimuli. A neural network model of how the perirhinal cortex could implement tong-term familiarity memory is proposed using Hebbian associative learning.

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

[2]  Stefano Panzeri,et al.  Information in the Neuronal Representation of Individual Stimuli in the Primate Temporal Visual Cortex , 1997, Journal of Computational Neuroscience.

[3]  J. Holdstock,et al.  The Quarterly Journal of Experimental Psychology , 2005 .

[4]  D. Gaffan,et al.  The hippocampus, perirhinal cortex and memory in the monkey , 2000 .

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

[6]  E. Rolls,et al.  Selective Perceptual Impairments After Perirhinal Cortex Ablation , 2001, The Journal of Neuroscience.

[7]  Gustavo Deco,et al.  Computational neuroscience of vision , 2002 .

[8]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

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

[10]  A. Treves,et al.  The representational capacity of the distributed encoding of information provided by populations of neurons in primate temporal visual cortex , 1997, Experimental Brain Research.

[11]  Edmund T. Rolls,et al.  The relative advantages of sparse versus distributed encoding for associative neuronal networks in the brain , 1990 .

[12]  K. Tanaka,et al.  Divergent Projections from the Anterior Inferotemporal Area TE to the Perirhinal and Entorhinal Cortices in the Macaque Monkey , 1996, The Journal of Neuroscience.

[13]  Y Miyashita,et al.  Feedback signal from medial temporal lobe mediates visual associative mnemonic codes of inferotemporal neurons. , 1996, Brain research. Cognitive brain research.

[14]  N. Mackintosh,et al.  Associative learning and elemental representation: II. Generalization and discrimination , 2002, Animal learning & behavior.

[15]  Edgar H Vogel,et al.  Stimulus representation in SOP: I Theoretical rationalization and some implications , 2003, Behavioural Processes.

[16]  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.

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

[18]  J. Houston Generalization and discrimination , 1981 .

[19]  Edgar H Vogel,et al.  Stimulus representation in SOP: II. An application to inhibition of delay , 2003, Behavioural Processes.

[20]  E. Oja Simplified neuron model as a principal component analyzer , 1982, Journal of mathematical biology.

[21]  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.

[22]  C. Malsburg,et al.  How patterned neural connections can be set up by self-organization , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[23]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Lisa M Saksida,et al.  The Perceptual-Mnemonic/Feature Conjunction Model of Perirhinal Cortex Function , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[25]  E. Rolls,et al.  Neural networks and brain function , 1998 .

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

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

[28]  Seth J. Ramus,et al.  Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system , 1994, Hippocampus.

[29]  E. Rolls Functions of the Primate Temporal Lobe Cortical Visual Areas in Invariant Visual Object and Face Recognition , 2000, Neuron.

[30]  R. Henson A Mini-Review of fMRI Studies of Human Medial Temporal Lobe Activity Associated with Recognition Memory , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[31]  M. W. Brown,et al.  Hippocampus and medial temporal cortex: Neuronal activity related to behavioural responses during the performance of memory tasks by primates , 1990, Behavioural Brain Research.

[32]  Christian Hölscher,et al.  Perirhinal cortex neuronal activity related to long‐term familiarity memory in the macaque , 2003, The European journal of neuroscience.

[33]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[34]  Yasushi Miyashita,et al.  Consolidation of Visual Associative Long-Term Memory in the Temporal Cortex of Primates , 1998, Neurobiology of Learning and Memory.

[35]  E. Rolls,et al.  Responses of neurons in the inferior temporal cortex in short term and serial recognition memory tasks , 2004, Experimental Brain Research.

[36]  M. Mishkin,et al.  Neurotoxic lesions of perirhinal cortex impair visual recognition memory in rhesus monkeys , 2001, Neuroreport.