Visual perception and memory: a new view of medial temporal lobe function in primates and rodents.

The prevailing view of medial temporal lobe (MTL) function has two principal elements: first, that the MTL subserves memory but not perception, and second, that the many anatomically distinctive parts of the MTL function together in the service of declarative memory. Recent neuropsychological studies have, however, challenged both opinions. First, studies in rodents, nonhuman primates, and humans suggest that the perirhinal cortex represents information about objects for both mnemonic and perceptual purposes. Second, the idea that MTL components contribute to declarative memory in similar ways has also been contradicted. Whereas the perirhinal cortex plays an essential role in familiarity-based object recognition, the hippocampus contributes little, if at all, to this function. In both primates and rodents, the hippocampus contributes to the memory and perception of places and paths, whereas the perirhinal cortex does so for objects and the contents of scenes.

[1]  E. Murray,et al.  Hippocampal Lesions in Rhesus Monkeys Disrupt Emotional Responses but Not Reinforcer Devaluation Effects , 2008, Biological Psychiatry.

[2]  Rosemary A. Cowell,et al.  Perceptual Functions of Perirhinal Cortex in Rats: Zero-Delay Object Recognition and Simultaneous Oddity Discriminations , 2007, The Journal of Neuroscience.

[3]  L. Saksida,et al.  Impairment and facilitation of transverse patterning after lesions of the perirhinal cortex and hippocampus, respectively. , 2006, Cerebral cortex.

[4]  Rosemary A. Cowell,et al.  Why Does Brain Damage Impair Memory? A Connectionist Model of Object Recognition Memory in Perirhinal Cortex , 2006, The Journal of Neuroscience.

[5]  Christian Schwarzbauer,et al.  Perirhinal cortex activity during visual object discrimination: An event-related fMRI study , 2006, NeuroImage.

[6]  J. Freeman,et al.  Perirhinal cortex lesions impair simultaneous but not serial feature-positive discrimination learning. , 2006, Behavioral neuroscience.

[7]  Andy C. H. Lee,et al.  Abnormal Categorization and Perceptual Learning in Patients with Hippocampal Damage , 2006, The Journal of Neuroscience.

[8]  Andy C. H. Lee,et al.  Differentiating the Roles of the Hippocampus and Perirhinal Cortex in Processes beyond Long-Term Declarative Memory: A Double Dissociation in Dementia , 2006, The Journal of Neuroscience.

[9]  David G. Amaral,et al.  Hippocampal Lesion Prevents Spatial Relational Learning in Adult Macaque Monkeys , 2006, The Journal of Neuroscience.

[10]  C. Lever,et al.  Effects of lesions to the dorsal and ventral hippocampus on defensive behaviors in rats , 2006, The European journal of neuroscience.

[11]  L. Saksida,et al.  Perirhinal cortex and feature-ambiguous discriminations. , 2006, Learning & memory.

[12]  Yael Shrager,et al.  Intact Visual Perception in Memory-Impaired Patients with Medial Temporal Lobe Lesions , 2006, The Journal of Neuroscience.

[13]  L. Saksida,et al.  No effect of hippocampal lesions on perirhinal cortex‐dependent feature‐ambiguous visual discriminations , 2006, Hippocampus.

[14]  Russell A. Epstein,et al.  Perceptual deficits in amnesia: challenging the medial temporal lobe ‘mnemonic’ view , 2005, Neuropsychologia.

[15]  L. Saksida,et al.  Object memory and perception in the medial temporal lobe: an alternative approach , 2005, Current Opinion in Neurobiology.

[16]  Andy C. H. Lee,et al.  Behavioral / Systems / Cognitive Functional Specialization in the Human Medial Temporal Lobe , 2005 .

[17]  K. Norman,et al.  Memory Strength and Repetition Suppression: Multimodal Imaging of Medial Temporal Cortical Contributions to Recognition , 2005, Neuron.

[18]  Robert R Hampton,et al.  Monkey Perirhinal Cortex is Critical for Visual Memory, but not for Visual Perception: Reexamination of the Behavioural Evidence from Monkeys , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[19]  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.

[20]  Jocelyne Bachevalier,et al.  Comparison of the Effects of Damage to the Perirhinal and Parahippocampal Cortex on Transverse Patterning and Location Memory in Rhesus Macaques , 2005, The Journal of Neuroscience.

[21]  Jocelyne Bachevalier,et al.  Selective neurotoxic damage to the hippocampal formation impairs performance of the transverse patterning and location memory tasks in rhesus macaques , 2005, Hippocampus.

[22]  L. Squire,et al.  Intact visual discrimination of complex and feature-ambiguous stimuli in the absence of perirhinal cortex. , 2005, Learning & memory.

[23]  T. Bussey,et al.  Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours , 2005, Hippocampus.

[24]  Andy C. H. Lee,et al.  Specialization in the medial temporal lobe for processing of objects and scenes , 2005, Hippocampus.

[25]  Sabrina M. Tom,et al.  Dissociable correlates of recollection and familiarity within the medial temporal lobes , 2004, Neuropsychologia.

[26]  Guy B. Williams,et al.  The human perirhinal cortex and semantic memory , 2004, The European journal of neuroscience.

[27]  Elisabeth A. Murray,et al.  What, if anything, is the medial temporal lobe, and how can the amygdala be part of it if there is no such thing? , 2004, Neurobiology of Learning and Memory.

[28]  Larry R Squire,et al.  Spatial memory, recognition memory, and the hippocampus. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  John P. Aggleton,et al.  When is the perirhinal cortex necessary for the performance of spatial memory tasks? , 2004, Neuroscience & Biobehavioral Reviews.

[30]  Rosemary A. Cowell,et al.  Double Dissociation between the Effects of Peri-Postrhinal Cortex and Hippocampal Lesions on Tests of Object Recognition and Spatial Memory: Heterogeneity of Function within the Temporal Lobe , 2004, The Journal of Neuroscience.

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

[32]  Derick H. Lindquist,et al.  Perirhinal Cortex Supports Delay Fear Conditioning to Rat Ultrasonic Social Signals , 2004, The Journal of Neuroscience.

[33]  R M Douglas,et al.  Visual memory task for rats reveals an essential role for hippocampus and perirhinal cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Maija Pihlajamäki,et al.  Visual presentation of novel objects and new spatial arrangements of objects differentially activates the medial temporal lobe subareas in humans , 2004, The European journal of neuroscience.

[35]  J. Rodd,et al.  Processing Objects at Different Levels of Specificity , 2004, Journal of Cognitive Neuroscience.

[36]  J. Bachevalier,et al.  The Hippocampal/Parahippocampal Regions and Recognition Memory: Insights from Visual Paired Comparison versus Object-Delayed Nonmatching in Monkeys , 2004, The Journal of Neuroscience.

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

[38]  M. Eacott,et al.  Impaired object recognition with increasing levels of feature ambiguity in rats with perirhinal cortex lesions , 2004, Behavioural Brain Research.

[39]  E. Murray,et al.  Selective hippocampal damage in rhesus monkeys impairs spatial memory in an open‐field test , 2004, Hippocampus.

[40]  J. Dalrymple-Alford,et al.  Perirhinal cortex and anterior thalamic lesions: comparative effects on learning and memory. , 2003, Behavioral neuroscience.

[41]  Paul E. Gilbert,et al.  Recognition memory for complex visual discriminations is influenced by stimulus interference in rodents with perirhinal cortex damage. , 2003, Learning & memory.

[42]  S P Wise,et al.  Role of the hippocampal system in associative learning beyond the spatial domain. , 2003, Brain : a journal of neurology.

[43]  J. Rawlins,et al.  Ventral hippocampal lesions affect anxiety but not spatial learning , 2003, Behavioural Brain Research.

[44]  Jason P. Mitchell,et al.  Multiple routes to memory: Distinct medial temporal lobe processes build item and source memories , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[45]  L. Saksida,et al.  Impairments in visual discrimination after perirhinal cortex lesions: testing ‘declarative’ vs. ‘perceptual‐mnemonic’ views of perirhinal cortex function , 2003, The European journal of neuroscience.

[46]  Andrew P Yonelinas,et al.  Dissociating familiarity from recollection in human recognition memory: Different rates of forgetting over short retention intervals , 2002, Psychonomic bulletin & review.

[47]  David Gaffan,et al.  Against memory systems. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[48]  M. Moser,et al.  Reduced fear expression after lesions of the ventral hippocampus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Robert R Hampton,et al.  Learning of discriminations is impaired, but generalization to altered views is intact, in monkeys (Macaca mulatta) with perirhinal cortex removal. , 2002, Behavioral neuroscience.

[50]  S. Corkin What's new with the amnesic patient H.M.? , 2002, Nature Reviews Neuroscience.

[51]  L. Saksida,et al.  Perirhinal cortex resolves feature ambiguity in complex visual discriminations , 2002, The European journal of neuroscience.

[52]  L. Saksida,et al.  The organization of visual object representations: a connectionist model of effects of lesions in perirhinal cortex , 2002, The European journal of neuroscience.

[53]  The 'what' and 'where' of event memory: Independence and interactivity within the medial temporal lobe , 2002 .

[54]  J. Rawlins,et al.  Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. , 2002, Behavioral neuroscience.

[55]  R. O’Reilly,et al.  Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? , 2002, Hippocampus.

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

[57]  M. Eacott,et al.  Elemental and configural visual discrimination learning following lesions to perirhinal cortex in the rat , 2001, Behavioural Brain Research.

[58]  R. Burwell Borders and cytoarchitecture of the perirhinal and postrhinal cortices in the rat , 2001, The Journal of comparative neurology.

[59]  Muge M. Bakircioglu,et al.  Mapping visual cortex in monkeys and humans using surface-based atlases , 2001, Vision Research.

[60]  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.

[61]  E. Murray,et al.  Opposite relationship of hippocampal and rhinal cortex damage to delayed nonmatching‐to‐sample deficits in monkeys † , 2001, Hippocampus.

[62]  E. Murray,et al.  Effects of hippocampal lesions on delayed nonmatching‐to‐sample in monkeys: A reply to Zola and Squire (2001) † , 2001, Hippocampus.

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

[64]  R. Clark,et al.  Rats with lesions of the hippocampus are impaired on the delayed nonmatching‐to‐sample task † , 2001, Hippocampus.

[65]  S. Gutnikov,et al.  Perceptual and Mnemonic Matching-To-Sample in Humans: Contributions of The Hippocampus, Perirhinal and Other Medial Temporal Lobe Cortices , 2000, Cortex.

[66]  Robert E. Clark,et al.  Impaired Recognition Memory in Rats after Damage to the Hippocampus , 2000, The Journal of Neuroscience.

[67]  John P. Aggleton,et al.  Intact negative patterning in rats with fornix or combined perirhinal and postrhinal cortex lesions , 2000, Experimental Brain Research.

[68]  Seth J. Ramus,et al.  Dissociation between the effects of damage to perirhinal cortex and area TE. , 1999, Learning & memory.

[69]  M. Chun,et al.  Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage , 1999, Nature Neuroscience.

[70]  P. Liu,et al.  The effect of excitotoxic lesions centered on the perirhinal cortex in two versions of the radial arm maze task. , 1999, Behavioral neuroscience.

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

[72]  Russell A. Epstein,et al.  The Parahippocampal Place Area Recognition, Navigation, or Encoding? , 1999, Neuron.

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

[74]  R. Killiany,et al.  Hippocampal formation lesions produce memory impairment in the rhesus monkey , 1999, Hippocampus.

[75]  E. Murray,et al.  Monkeys with rhinal cortex damage or neurotoxic hippocampal lesions are impaired on spatial scene learning and object reversals. , 1998, Behavioral neuroscience.

[76]  M. Mishkin,et al.  Object Recognition and Location Memory in Monkeys with Excitotoxic Lesions of the Amygdala and Hippocampus , 1998, The Journal of Neuroscience.

[77]  P. Liu,et al.  Excitotoxic lesions centered on perirhinal cortex produce delay-dependent deficits in a test of spatial memory. , 1998, Behavioral neuroscience.

[78]  P. Liu,et al.  Perirhinal cortex contributions to performance in the Morris water maze. , 1998, Behavioral neuroscience.

[79]  Alex Martin,et al.  Properties and mechanisms of perceptual priming , 1998, Current Opinion in Neurobiology.

[80]  T. Bussey,et al.  Fornix Lesions Can Facilitate Acquisition of the Transverse Patterning Task: A Challenge for “Configural” Theories of Hippocampal Function , 1998, The Journal of Neuroscience.

[81]  D. Schacter,et al.  Priming and the Brain , 1998, Neuron.

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

[83]  D. Bilkey,et al.  Lesions of perirhinal cortex produce spatial memory deficits in the radial maze , 1998, Hippocampus.

[84]  M. Mishkin,et al.  Differential effects of early hippocampal pathology on episodic and semantic memory. , 1997, Science.

[85]  D. Gaffan,et al.  Impairment of visual object-discrimination learning after perirhinal cortex ablation. , 1997, Behavioral neuroscience.

[86]  E. Murray,et al.  Functional double dissociation between two inferior temporal cortical areas: perirhinal cortex versus middle temporal gyrus. , 1997, Journal of neurophysiology.

[87]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[89]  L. Nadel The role of the hippocampus in declarative memory: A comment on Zola‐Morgan, Squire, and Ramus (1994) , 1995, Hippocampus.

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

[91]  E. Murray,et al.  Preserved Recognition Memory for Small Sets, and Impaired Stimulus Identification for Large Sets, Following Rhinal Cortex Ablations in Monkeys , 1994, The European journal of neuroscience.

[92]  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.

[93]  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.

[94]  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.

[95]  E. Tulving Elements of episodic memory , 1983 .

[96]  L. Radinsky THE FOSSIL RECORD OF PRIMATE BRAIN EVOLUTION , 1979 .

[97]  D. Hooker JAMES ARTHUR LECTURE ON THE EVOLUTION OF THE HUMAN BRAIN , 1958 .

[98]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.