The rat perirhinal cortex: A review of anatomy, physiology, plasticity, and function

The perirhinal cortex is located in a pivotal position to influence the flow of information into and out of the hippocampal formation. In this review, we examine the anatomical, physiological and functional properties of the rat perirhinal cortex. Firstly, we review the properties of the perirhinal cortex itself, we describe how it can be separated into two distinct subregions and consider how it differs from other neighbouring regions in terms of cell type, cellular organisation and its afferent and efferent projections. We review the forms of neurotransmission present in the perirhinal cortex and the morphological, electrophysiological and plastic properties of its neurons. Secondly, we review the perirhinal cortex in the context of its connections with other brain areas; focussing on the projections to cortical, subcortical and hippocampal/parahippocampal regions. Particular attention is paid the anatomical and electrophysiological properties of these projections. Thirdly, we review the main functions of the perirhinal cortex; its roles in perception, recognition memory, spatial and contextual memory and fear conditioning are explored. Finally, we discuss the idea of anatomical, electrophysiological and functional segregation within the perirhinal cortex itself and as part of a hippocampal-parahippocampal network and suggest that understanding this segregation is of critical importance in understanding the role and contributions made by the perirhinal cortex in general.

[1]  Malcolm W. Brown,et al.  Recognition memory: Material, processes, and substrates , 2010, Hippocampus.

[2]  J. Siuciak,et al.  In Situ Hybridization of trkB and trkC Receptor mRNA in Rat Forebrain and Association with High‐affinity Binding of [125I]BDNF, [125I]NT‐4/5 and [125I]NT‐3 , 1994, The European journal of neuroscience.

[3]  Abdelkader Ennaceur,et al.  Effects of physostigmine and scopolamine on rats' performances in object-recognition and radial-maze tests , 1992, Psychopharmacology.

[4]  A. Pertovaara,et al.  Influence of amygdaloid glutamatergic receptors on sensory and emotional pain-related behavior in the neuropathic rat , 2010, Behavioural Brain Research.

[5]  J. Pearce,et al.  Neurotoxic lesions of the rat perirhinal and postrhinal cortices and their impact on biconditional visual discrimination tasks , 2007, Behavioural Brain Research.

[6]  M. W. Brown,et al.  Neuronal Sianallina of Information Imoortant to Visual Recognition‐Memory in Rat Rhinal aid Neighbouring Cortices , 1995, The European journal of neuroscience.

[7]  L. Saksida,et al.  Visual perception and memory: a new view of medial temporal lobe function in primates and rodents. , 2007, Annual review of neuroscience.

[8]  T. Otto,et al.  Induction and transient suppression of long-term potentiation in the peri- and postrhinal cortices following theta-related stimulation of hippocampal field CA1 , 1998, Brain Research.

[9]  N. Mizuno,et al.  Collateral projections of single neurons in the posterior thalamic region to both the temporal cortex and the amygdala: a fluorescent retrograde double‐labeling study in the rat , 1997, The Journal of comparative neurology.

[10]  D K Bilkey,et al.  Is there a direct projection from perirhinal cortex to the hippocampus? , 1998, Hippocampus.

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

[12]  K. Felszeghy,et al.  Selective decline of 5-HT1A receptor binding sites in rat cortex, hippocampus and cholinergic basal forebrain nuclei during aging , 1997, Journal of Chemical Neuroanatomy.

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

[14]  T. Bussey,et al.  Extensive Cytotoxic Lesions Involving Both the Rhinal Cortices and Area TE Impair Recognition But Spare Spatial Alternation in the Rat , 1997, Brain Research Bulletin.

[15]  Bruno Poucet,et al.  Role of the parietal cortex in long-term representation of spatial information in the rat , 2009, Neurobiology of Learning and Memory.

[16]  R. Burwell,et al.  Positional firing properties of postrhinal cortex neurons , 2003, Neuroscience.

[17]  M. Zhuo,et al.  Roles of NMDA receptor NR2A and NR2B subtypes for long‐term depression in the anterior cingulate cortex , 2005, The European journal of neuroscience.

[18]  G. Niewiadomska,et al.  Nerve Growth Factor Differentially Affects Spatial and Recognition Memory in Aged Rats , 2006, Neurochemical Research.

[19]  E. Save,et al.  Hippocampal‐parietal cortical interactions in spatial cognition , 2000, Hippocampus.

[20]  Rosemary A. Cowell,et al.  Heightened susceptibility to interference in an animal model of amnesia: Impairment in encoding, storage, retrieval – or all three? , 2010, Neuropsychologia.

[21]  David J. Bucci,et al.  Posterior parietal cortex: An interface between attention and learning? , 2009, Neurobiology of Learning and Memory.

[22]  M. Barbacid,et al.  The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain , 1990, Cell.

[23]  E. D. Leonibus,et al.  Co-activation of glutamate and dopamine receptors within the nucleus accumbens is required for spatial memory consolidation in mice , 2005, Psychopharmacology.

[24]  O. Steward,et al.  Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat , 1976, The Journal of comparative neurology.

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

[26]  David K. Bilkey,et al.  Characterization of epileptiform field potentials recorded in the in vitro perirhinal cortex of amygdala-kindled epileptogenesis , 1996, Brain Research.

[27]  M. Witter,et al.  What Does the Anatomical Organization of the Entorhinal Cortex Tell Us? , 2008, Neural plasticity.

[28]  H. Markowitsch,et al.  Cortical and thalamic afferent connections of the insular and adjacent cortex of the cat , 1983, The Journal of comparative neurology.

[29]  V. Bertaina-Anglade,et al.  The object recognition task in rats and mice: a simple and rapid model in safety pharmacology to detect amnesic properties of a new chemical entity. , 2006, Journal of pharmacological and toxicological methods.

[30]  T. H. Brown,et al.  Single-Unit Firing in Rat Perirhinal Cortex Caused by Fear Conditioning to Arbitrary and Ecological Stimuli , 2007, The Journal of Neuroscience.

[31]  M. Bunsey,et al.  The effects of lesions to the rat hippocampus or rhinal cortex on olfactory and spatial memory: Retrograde and anterograde findings , 2001, Cognitive, affective & behavioral neuroscience.

[32]  E. Baldi,et al.  Differential contribution of some cortical sites to the formation of memory traces supporting fear conditioning , 2002, Experimental Brain Research.

[33]  D. Wilson,et al.  Receptive fields in the rat piriform cortex. , 2001, Chemical senses.

[34]  M. Eacott,et al.  Perirhinal cortex ablation in rats selectively impairs object identification in a simultaneous visual comparison task. , 2000, Behavioral neuroscience.

[35]  Rosemary A. Cowell,et al.  Functional Dissociations within the Ventral Object Processing Pathway: Cognitive Modules or a Hierarchical Continuum? , 2010, Journal of Cognitive Neuroscience.

[36]  Z. Bashir,et al.  Benzodiazepine impairment of perirhinal cortical plasticity and recognition memory , 2004, The European journal of neuroscience.

[37]  M. Witter,et al.  Cingulate cortex projections to the parahippocampal region and hippocampal formation in the rat , 2007, Hippocampus.

[38]  T. H. Brown,et al.  Auditory trace fear conditioning requires perirhinal cortex , 2008, Neurobiology of Learning and Memory.

[39]  G. V. Hoesen,et al.  A direct projection from the perirhinal cortex (area 35) to the subiculum in the rat , 1983, Brain Research.

[40]  M. Buckley The Role of the Perirhinal Cortex and Hippocampus in Learning, Memory, and Perception , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[41]  John P. Aggleton,et al.  Interleaving brain systems for episodic and recognition memory , 2006, Trends in Cognitive Sciences.

[42]  S. Heldt,et al.  Lesions of the perirhinal cortex interfere with conditioned excitation but not with conditioned inhibition of fear. , 1997, Behavioral neuroscience.

[43]  D. Mcintyre,et al.  Perirhinal cortex involvement in limbic kindled seizures , 1996, Epilepsy Research.

[44]  J. T. Erichsen,et al.  Fos Imaging Reveals Differential Patterns of Hippocampal and Parahippocampal Subfield Activation in Rats in Response to Different Spatial Memory Tests , 2000, The Journal of Neuroscience.

[45]  J. Aggleton,et al.  Spontaneous recognition of object configurations in rats: effects of fornix lesions , 1994, Experimental Brain Research.

[46]  T. Myhrer Effects of Selective Perirhinal and Postrhinal Lesions on Acquisition and Retention of a Visual Discrimination Task in Rats , 2000, Neurobiology of Learning and Memory.

[47]  J. Aggleton,et al.  The Different Effects on Recognition Memory of Perirhinal Kainate and NMDA Glutamate Receptor Antagonism: Implications for Underlying Plasticity Mechanisms , 2006, The Journal of Neuroscience.

[48]  Sarah Craig,et al.  The subiculum to entorhinal cortex projection is capable of sustaining both short- and long-term plastic changes , 2006, Behavioural Brain Research.

[49]  D. Bilkey,et al.  Lesions of rat perirhinal cortex exacerbate the memory deficit observed following damage to the fimbria-fornix. , 1995, Behavioral neuroscience.

[50]  L. Saksida,et al.  Rats spontaneously discriminate purely visual, two-dimensional stimuli in tests of recognition memory and perceptual oddity. , 2007, Behavioral neuroscience.

[51]  C. Beltramino,et al.  Facilitatory and inhibitory effects of electrochemical stimulation of the amygdala on the release of luteinizing hormone , 1978, Brain Research.

[52]  M. Brandão,et al.  Midazolam reduces the selective activation of the rhinal cortex by contextual fear stimuli , 2011, Behavioural Brain Research.

[53]  J. Price,et al.  Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat , 1977, The Journal of comparative neurology.

[54]  T. H. Brown,et al.  Muscarinic Receptors in Perirhinal Cortex Control Trace Conditioning , 2009, The Journal of Neuroscience.

[55]  Sarah Craig,et al.  Plastic and metaplastic changes in the CA1 and subicular projections to the entorhinal cortex , 2007, Brain Research.

[56]  E. Grove,et al.  Neural associations of the substantia innominata in the rat: Afferent connections , 1988, The Journal of comparative neurology.

[57]  A. Loewy,et al.  CNS inputs to the suprachiasmatic nucleus of the rat , 2002, Neuroscience.

[58]  D. Mumby,et al.  Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. , 2002, Learning & memory.

[59]  John P. Aggleton,et al.  cAMP Responsive Element-Binding Protein Phosphorylation Is Necessary for Perirhinal Long-Term Potentiation and Recognition Memory , 2005, The Journal of Neuroscience.

[60]  T. H. Brown,et al.  Morphology and ontogeny of rat perirhinal cortical neurons , 2007, The Journal of comparative neurology.

[61]  J. Huston,et al.  Dissociating effects of cocaine and d-amphetamine on dopamine and serotonin in the perirhinal, entorhinal, and prefrontal cortex of freely moving rats , 2007, Psychopharmacology.

[62]  J. Tsien,et al.  Genetic Enhancement of Memory and Long-Term Potentiation but Not CA1 Long-Term Depression in NR2B Transgenic Rats , 2009, PloS one.

[63]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[64]  R. Vertes,et al.  Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat , 2007, Brain Structure and Function.

[65]  L. Swanson,et al.  Organization of projections from the ventromedial nucleus of the hypothalamus: A Phaseolus vulgaris‐Leucoagglutinin study in the rat , 1994, The Journal of comparative neurology.

[66]  Z. Bashir,et al.  Activation of muscarinic receptors induces protein synthesis‐dependent long‐lasting depression in the perirhinal cortex , 2001, The European journal of neuroscience.

[67]  W. Cowan,et al.  Evidence for collateral projections by neurons in Ammon's horn, the dentate gyrus, and the subiculum: a multiple retrograde labeling study in the rat , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  M. T. Shipley,et al.  CHAPTER 29 – Olfactory System , 2004 .

[69]  B. Vogt,et al.  Direct connections of rat visual cortex with sensory, motor, and association cortices , 1984, The Journal of comparative neurology.

[70]  T. Reader,et al.  Effects of chronic antidepressant treatments on 5-HT and NA transporters in rat brain: an autoradiographic study , 2001, Neurochemistry International.

[71]  M. Cossette,et al.  A limited role for the hippocampus in the modulation of novel-object preference by contextual cues. , 2008, Learning & memory.

[72]  M. W. Brown,et al.  Synaptic depression induced by pharmacological activation of metabotropic glutamate receptors in the perirhinal cortex in vitro , 1999, Neuroscience.

[73]  Riichi Kajiwara,et al.  Convergence of entorhinal and CA3 inputs onto pyramidal neurons and interneurons in hippocampal area CA1—An anatomical study in the rat , 2008, Hippocampus.

[74]  M. J. Christie,et al.  Excitatory amino acid projections to the nucleus accumbens septi in the rat: A retrograde transport study utilizingd[3H]aspartate and [3H]GABA , 1987, Neuroscience.

[75]  E. Mufson,et al.  Retrograde transport of brain‐derived neurotrophic factor (BDNF) following infusion in neo‐and limbic cortex in rat: Relationship to BDNF mRNA expressing neurons , 1996, The Journal of comparative neurology.

[76]  A. Pitkänen,et al.  Projections from the lateral, basal and accessory basal nuclei of the amygdala to the perirhinal and postrhinal cortices in rat. , 2001, Cerebral cortex.

[77]  F. H. Lopes da Silva,et al.  Evidence for a direct projection from the postrhinal cortex to the subiculum in the rat , 2001, Hippocampus.

[78]  Stephen Maren,et al.  Long-term potentiation in the amygdala: a mechanism for emotional learning and memory , 1999, Trends in Neurosciences.

[79]  L. Kelly,et al.  Long-term retention and overshadowing of proximal and distal cues following habituation in an object exploration task , 2005, Behavioural Processes.

[80]  Michael Davis,et al.  Neural systems involved in fear and anxiety measured with fear-potentiated startle. , 2006, The American psychologist.

[81]  L. Nerad,et al.  Bilateral NMDA lesions centered on the postrhinal cortex have minimal effects on hippocampal place cell firing , 2009, Hippocampus.

[82]  Malcolm W. Brown,et al.  Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory , 2010, Neuropsychologia.

[83]  J. Delacour,et al.  A new one-trial test for neurobiological studies of memory in rats. II: Effects of piracetam and pramiracetam , 1989, Behavioural Brain Research.

[84]  M. J. Christie,et al.  Excitatory amino acid projections to the periaqueductal gray in the rat: A retrograde transport study utilizing d[3H]aspartate and [3H]GABA , 1990, Neuroscience.

[85]  Malcolm W. Brown,et al.  Cholinergic Neurotransmission Is Essential for Perirhinal Cortical Plasticity and Recognition Memory , 2003, Neuron.

[86]  J. Muir,et al.  Neurotoxic lesions of the rat perirhinal cortex fail to disrupt the acquisition or performance of tests of allocentric spatial memory. , 2002, Behavioral neuroscience.

[87]  R. D. BURWELLa,et al.  POSITIONAL FIRING PROPERTIES OF POSTRHINAL CORTEX NEURONS , 2003 .

[88]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: Interconnectivity and connections with the entorhinal cortex , 1998, The Journal of comparative neurology.

[89]  M. de Curtis,et al.  Functional interactions within the parahippocampal region revealed by voltage-sensitive dye imaging in the isolated guinea pig brain. , 2010, Journal of neurophysiology.

[90]  J. Mong,et al.  Methamphetamine enhances paced mating behaviors and neuroplasticity in the medial amygdala of female rats , 2010, Hormones and Behavior.

[91]  Perirhinal cortex relays auditory information to the frontal motor cortices in the rat , 2003, Neuroscience Letters.

[92]  Joseph E LeDoux,et al.  A gradient of plasticity in the amygdala revealed by cortical and subcortical stimulation, in vivo , 2001, Neuroscience.

[93]  D. Mumby,et al.  Perirhinal cortex lesions produce variable patterns of retrograde amnesia in rats , 2003, Behavioural Brain Research.

[94]  Brigitte Schulz-Klaus Neurotoxic lesion of the rostral perirhinal cortex blocks stress-induced exploratory behavioral changes in male rats , 2009, Stress.

[95]  T. H. Brown,et al.  Predominance of Late-Spiking Neurons in Layer VI of Rat Perirhinal Cortex , 2001, The Journal of Neuroscience.

[96]  R. Linke Organization of projections to temporal cortex originating in the thalamic posterior intralaminar nucleus of the rat , 1999, Experimental Brain Research.

[97]  Shane M. O'Mara,et al.  Blockade of NMDA receptors pre-training, but not post-training, impairs object displacement learning in the rat , 2008, Brain Research.

[98]  Douglas Nitz,et al.  Parietal cortex, navigation, and the construction of arbitrary reference frames for spatial information , 2009, Neurobiology of Learning and Memory.

[99]  K. Gale,et al.  Immunohistochemical evaluation of the protein expression of nerve growth factor and its TrkA receptor in rat limbic regions following electroshock seizures , 2009, Neuroscience Research.

[100]  J. Aggleton,et al.  The effects of cytotoxic perirhinal cortex lesions on spatial learning by rats: a comparison of the dark agouti and Sprague-Dawley strains. , 2006, Behavioral neuroscience.

[101]  John M. Beggs,et al.  Prolonged synaptic integration in perirhinal cortical neurons. , 2000, Journal of neurophysiology.

[102]  J. Joyce,et al.  Dopamine D2 receptor expression in hippocampus and parahippocampal cortex of rat, cat, and human in relation to tyrosine hydroxylase‐immunoreactive fibers , 1994, Hippocampus.

[103]  T. Kosaka,et al.  Tyrosine hydroxylase-immunoreactive intrinsic neurons in the rat cerebral cortex , 2004, Experimental Brain Research.

[104]  G. Collingridge,et al.  The NMDA Receptor , 1995 .

[105]  M. W. Brown,et al.  Novel spatial arrangements of familiar visual stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices: a c-fos expression study , 2004, Neuroscience.

[106]  D. Paré,et al.  The rhinal cortices: a wall of inhibition between the neocortex and the hippocampus , 2004, Progress in Neurobiology.

[107]  A. Shyu,et al.  Expression of NGFI-B mRNA in a rat focal cerebral ischemia-reperfusion model. , 1996, Brain research. Molecular brain research.

[108]  E. Richfield,et al.  Comparative distributions of dopamine D‐1 and D‐2 receptors in the cerebral cortex of rats, cats, and monkeys , 1989, The Journal of comparative neurology.

[109]  L. Ricceri,et al.  NGF induces appearance of adult-like response to spatial novelty in 18-day male mice , 2002, Behavioural Brain Research.

[110]  George Paxinos,et al.  CHAPTER 34 – The Serotonin and Tachykinin Systems , 2004 .

[111]  D. Mumby,et al.  Dissociation in retrograde memory for object discriminations and object recognition in rats with perirhinal cortex damage , 2002, Behavioural Brain Research.

[112]  J. Rosen,et al.  Animal studies of amygdala function in fear and uncertainty: Relevance to human research , 2006, Biological Psychology.

[113]  Perirhinal cortex does not project to the dentate gyrus , 1999, Hippocampus.

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

[115]  D. Arnold,et al.  Mesial temporal damage in temporal lobe epilepsy: a volumetric MRI study of the hippocampus, amygdala and parahippocampal region. , 2003, Brain : a journal of neurology.

[116]  M. Witter,et al.  Projection from the nucleus reuniens thalami to the hippocampal region: Light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris‐leucoagglutinin , 1990, The Journal of comparative neurology.

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

[118]  O. Steward,et al.  Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat , 1976, The Journal of comparative neurology.

[119]  Garrett E. Alexander Basal ganglia , 1998 .

[120]  J. Aggleton,et al.  Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix , 1997, Experimental Brain Research.

[121]  H. Markowitsch,et al.  Cortical and thalamic afferent connections of the insular and adjacent cortex of the rat , 1983, The Journal of comparative neurology.

[122]  G. Collingridge,et al.  Metabotropic Glutamate Receptor-Mediated LTD Involves Two Interacting Ca2+ Sensors, NCS-1 and PICK1 , 2008, Neuron.

[123]  H. Carrer,et al.  New facts concerning the role played by the ventromedial nucleus in the control of estrous cycle duration and sexual receptivity in the rat. , 1973, Neuroendocrinology.

[124]  A. Pitkänen,et al.  Projections from the periamygdaloid cortex to the amygdaloid complex, the hippocampal formation, and the parahippocampal region: A PHA‐L study in the rat , 2003, Hippocampus.

[125]  T. H. Brown,et al.  Perirhinal cortex supports acquired fear of auditory objects , 2009, Neurobiology of Learning and Memory.

[126]  R. C. Honey,et al.  Lesions of the perirhinal cortex do not impair integration of visual and geometric information in rats. , 2010, Behavioral neuroscience.

[127]  T. Bussey,et al.  Glutamate Receptors in Perirhinal Cortex Mediate Encoding, Retrieval, and Consolidation of Object Recognition Memory , 2005, The Journal of Neuroscience.

[128]  A. Guidotti,et al.  Reversible Modification of GABAA Receptor Subunit mRNA Expression During Tolerance to Diazepam-induced Cognition Dysfunction , 1996, Neuropharmacology.

[129]  O. Phillipson,et al.  The topographic order of inputs to nucleus accumbens in the rat , 1985, Neuroscience.

[130]  H. Groenewegen,et al.  The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics , 2003, Neuroscience & Biobehavioral Reviews.

[131]  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.

[132]  R. Vertes,et al.  Afferent projections to nucleus reuniens of the thalamus , 2004, The Journal of comparative neurology.

[133]  F. H. Lopes da Silva,et al.  Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum , 2001, Hippocampus.

[134]  L. Squire,et al.  Constructing receiver operating characteristics (ROCs) with experimental animals: cautionary notes. , 2008, Learning & memory.

[135]  J. Aggleton,et al.  Identifying cortical inputs to the rat hippocampus that subserve allocentric spatial processes: A simple problem with a complex answer , 2000, Hippocampus.

[136]  L. Swanson,et al.  Organization of projections from the basomedial nucleus of the amygdala: A PHAL study in the rat , 1996, The Journal of comparative neurology.

[137]  I. Izquierdo,et al.  Cholinergic Neurotransmission and Synaptic Plasticity Concerning Memory Processing , 1997, Neurochemical Research.

[138]  S. Rauch,et al.  Fear extinction in rats: Implications for human brain imaging and anxiety disorders , 2006, Biological Psychology.

[139]  M. Gallagher,et al.  Entorhinal-perirhinal lesions impair performance of rats on two versions of place learning in the Morris water maze. , 1995, Behavioral neuroscience.

[140]  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.

[141]  Jaak Panksepp,et al.  Neuroevolutionary sources of laughter and social joy: Modeling primal human laughter in laboratory rats , 2007, Behavioural Brain Research.

[142]  Menno P. Witter,et al.  The parahippocampal region: past, present, and future , 2002 .

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

[144]  H. Schnitzler,et al.  Temporary inactivation of the rostral perirhinal cortex induces an anxiolytic-like effect on the elevated plus-maze and on the yohimbine-enhanced startle response , 2005, Behavioural Brain Research.

[145]  S. Commins,et al.  Frequency-dependent changes in synaptic plasticity and brain-derived neurotrophic factor (BDNF) expression in the CA1 to perirhinal cortex projection , 2010, Brain Research.

[146]  M. Davis,et al.  Lesions of the perirhinal cortex but not of the frontal, medial prefrontal, visual, or insular cortex block fear-potentiated startle using a visual conditioned stimulus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[148]  Neda Bernasconi,et al.  Entorhinal Cortex MRI Assessment in Temporal, Extratemporal, and Idiopathic Generalized Epilepsy , 2003, Epilepsia.

[149]  J. Delacour,et al.  A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data , 1988, Behavioural Brain Research.

[150]  M. Witter,et al.  Topographical and laminar organization of subicular projections to the parahippocampal region of the rat , 2003, The Journal of comparative neurology.

[151]  James L. McClelland,et al.  Neural models of memory , 1999, Current Opinion in Neurobiology.

[152]  Z. Bashir,et al.  Learning-Specific Changes in Long-Term Depression in Adult Perirhinal Cortex , 2008, The Journal of Neuroscience.

[153]  M. Davis,et al.  Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[154]  R. Roesler,et al.  Pre- or post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats , 2005, Behavioural Brain Research.

[155]  J. Aggleton,et al.  Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat , 1996, Behavioural Brain Research.

[156]  Hal Blumenfeld,et al.  Is Epilepsy a Preventable Disorder? New Evidence from Animal Models , 2010, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[157]  M. Witter,et al.  Differential distribution of barrel or visual cortex Evoked responses along the rostro-caudal axis of the peri- and postrhinal cortices , 2000, Brain Research.

[158]  Z. Bashir,et al.  L-Type Voltage-Dependent Calcium Channel Antagonists Impair Perirhinal Long-Term Recognition Memory and Plasticity Processes , 2009, The Journal of Neuroscience.

[159]  F. Mascagni,et al.  Cortico-cortical and cortico-amygdaloid projections of the rat occipital cortex: a Phaseolus vulgaris leucoagglutinin study , 1996, Neuroscience.

[160]  M. Eacott,et al.  The role of perirhinal cortex in visual discrimination learning for visual secondary reinforcement in rats. , 2003, Behavioral neuroscience.

[161]  L. Haberly,et al.  Intrinsic and efferent connections of the endopiriform nucleus in rat , 1999, The Journal of comparative neurology.

[162]  T. Otto,et al.  Contributions of anterior perirhinal cortex to olfactory and contextual fear conditioning , 1998, Neuroreport.

[163]  Z. Bashir,et al.  Experience-dependent modification of mechanisms of long-term depression , 2006, Nature Neuroscience.

[164]  M. VanElzakker,et al.  Environmental novelty is associated with a selective increase in Fos expression in the output elements of the hippocampal formation and the perirhinal cortex. , 2008, Learning & memory.

[165]  M. de Curtis,et al.  Olfactory input to the parahippocampal region of the isolated guinea pig brain reveals weak entorhinal‐to‐perirhinal interactions , 2003, The European journal of neuroscience.

[166]  José María Delgado-García,et al.  From learning to forgetting: Behavioral, circuitry, and molecular properties define the different functional states of the recognition memory trace , 2010, Hippocampus.

[167]  Z. Bashir,et al.  Metabotropic glutamate receptor signalling in perirhinal cortical neurons , 2004, Molecular and Cellular Neuroscience.

[168]  R. Racine,et al.  Long‐term potentiation in the reciprocal corticohippocampal and corticocortical pathways in the chronically implanted, freely moving rat , 2000, Hippocampus.

[169]  Joseph E LeDoux,et al.  Bilateral destruction of neocortical and perirhinal projection targets of the acoustic thalamus does not disrupt auditory fear conditioning , 1992, Neuroscience Letters.

[170]  D. Bilkey,et al.  Direct connection between perirhinal cortex and hippocampus is a major constituent of the lateral perforant path , 1998, Hippocampus.

[171]  A. Ennaceur,et al.  A new one-trial test for neurobiological studies of memory in rats. III. Spatial vs. non-spatial working memory , 1992, Behavioural Brain Research.

[172]  H. Shibata Direct projections from the anterior thalamic nuclei to the retrohippocampal region in the rat , 1993, The Journal of comparative neurology.

[173]  Inah Lee,et al.  Disconnection of the Hippocampal–Perirhinal Cortical Circuits Severely Disrupts Object–Place Paired Associative Memory , 2010, The Journal of Neuroscience.

[174]  F. H. Lopes da Silva,et al.  Two reentrant pathways in the hippocampal‐entorhinal system , 2004, Hippocampus.

[175]  Jacki Y. Brown,et al.  Aberrant cortical synaptic plasticity and dopaminergic dysfunction in a mouse model of Huntington's disease. , 2006, Human molecular genetics.

[176]  M. E. Corcoran,et al.  Anterior perirhinal cortex kindling produces long‐lasting effects on anxiety and object recognition memory , 2005, The European journal of neuroscience.

[177]  M. Eacott,et al.  The Roles of Perirhinal Cortex, Postrhinal Cortex, and the Fornix in Memory for Objects, Contexts, and Events in the Rat , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[178]  C. Saper,et al.  Efferent projections of the infralimbic cortex of the rat , 1991, The Journal of comparative neurology.

[179]  Michael J. Jutras,et al.  Perirhinal and Postrhinal Contributions to Remote Memory for Context , 2004, The Journal of Neuroscience.

[180]  R. Stackman,et al.  On the delay-dependent involvement of the hippocampus in object recognition memory , 2004, Neurobiology of Learning and Memory.

[181]  T. Otto,et al.  Odor-guided fear conditioning in rats: 2. Lesions of the anterior perirhinal cortex disrupt fear conditioned to the explicit conditioned stimulus but not to the training context. , 1997, Behavioral neuroscience.

[182]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

[183]  D. Riccio,et al.  Olfactory learning and memory impairments following lesions to the hippocampus and perirhinal-entorhinal cortex. , 2003, Behavioral neuroscience.

[184]  Rosemary A. Cowell,et al.  Perirhinal cortex resolves feature ambiguity in configural object recognition and perceptual oddity tasks. , 2007, Learning & memory.

[185]  É. Griffin,et al.  Exercise enhances hippocampal‐dependent learning in the rat: Evidence for a BDNF‐related mechanism , 2009, Hippocampus.

[186]  O. Swezy THE ALBINO RAT. , 1928, Science.

[187]  C. Altar,et al.  Brain dopamine and serotonin receptor sites revealed by digital subtraction autoradiography. , 1985, Science.

[188]  O. Lindvall,et al.  Regulation of neurotrophin and traka, trkb and trkc tyrosine kinase receptor messenger RNA expression in kindling , 1993, Neuroscience.

[189]  L. Heimer,et al.  Efferent connections of the caudal part of the globus pallidus in the rat , 1996, The Journal of comparative neurology.

[190]  S. J. Shammah-Lagnado,et al.  Afferent connections of the amygdalopiriform transition area in the rat , 2005, The Journal of comparative neurology.

[191]  L. Saksida,et al.  The touchscreen cognitive testing method for rodents: how to get the best out of your rat. , 2008, Learning & memory.

[192]  G. V. Hoesen,et al.  Non-hippocampal cortical projections from the entorhinal cortex in the rat and rhesus monkey , 1982, Brain Research.

[193]  H. Schnitzler,et al.  Temporary inactivation of the perirhinal cortex by muscimol injections block acquisition and expression of fear‐potentiated startle , 2004, The European journal of neuroscience.

[194]  Hiroshi Abe,et al.  NMDA and muscarinic blockade in the perirhinal cortex impairs object discrimination in rats , 2001, Neuroreport.

[195]  J. Aggleton,et al.  Magnitude of the object recognition deficit associated with perirhinal cortex damage in rats: Effects of varying the lesion extent and the duration of the sample period. , 2009, Behavioral neuroscience.

[196]  Z. Bashir,et al.  A temporally distinct role for group I and group II metabotropic glutamate receptors in object recognition memory. , 2006, Learning & memory.

[197]  Malcolm W. Brown,et al.  Contrasting Hippocampal and Perirhinalcortex Function using Immediate Early Gene Imaging , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[198]  J. Monti The role of dorsal raphe nucleus serotonergic and non-serotonergic neurons, and of their receptors, in regulating waking and rapid eye movement (REM) sleep. , 2010, Sleep medicine reviews.

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

[200]  J. Henley,et al.  Differential redistribution of native AMPA receptor complexes following LTD induction in acute hippocampal slices , 2007, Neuropharmacology.

[201]  Andrew L. Gundlach,et al.  Quantitative autoradiographic localization in rat brain of α 2-adrenergic and non-adrenergic I-receptor binding sites labelled by [3H]rilmenidine , 1995, Brain Research.

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

[203]  Sarah Craig,et al.  Interaction between paired-pulse facilitation and long-term potentiation in the projection from hippocampal area CA1 to the entorhinal cortex , 2005, Neuroscience Research.

[204]  W. Krieg Connections of the cerebral cortex. I. The albino rat. B. Structure of the cortical areas , 1946, The Journal of comparative neurology.

[205]  J. Nierenberg,et al.  A Role for the Bilateral Involvement of Perirhinal Cortex in Generalized Kindled Seizure Expression , 1998, Experimental Neurology.

[206]  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.

[207]  D. Mumby,et al.  Place memory is intact in rats with perirhinal cortex lesions. , 1998, Behavioral neuroscience.

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

[209]  Boyer D Winters,et al.  A Distributed Cortical Representation Underlies Crossmodal Object Recognition in Rats , 2010, The Journal of Neuroscience.

[210]  M. Jouvet,et al.  Afferent projections to the rat nuclei raphe magnus, raphe pallidus and reticularis gigantocellularis pars α demonstrated by iontophoretic application of choleratoxin (subunit b) , 1997, Journal of Chemical Neuroanatomy.

[211]  John T Wixted,et al.  Measuring recollection and familiarity in the medial temporal lobe , 2010, Hippocampus.

[212]  T. Otto,et al.  Patterns of Fos expression in the amygdala and ventral perirhinal cortex induced by training in an olfactory fear conditioning paradigm. , 2001, Behavioral neuroscience.

[213]  J. T. Erichsen,et al.  Using Fos Imaging in the Rat to Reveal the Anatomical Extent of the Disruptive Effects of Fornix Lesions , 2000, The Journal of Neuroscience.

[214]  A. Carlsson,et al.  Differential effects of the N-methyl-d-aspartate receptor antagonist MK-801 on different stages of object recognition memory in mice , 2007, Neuroscience.

[215]  M. W. Brown,et al.  Differential activation of the rat hippocampus and perirhinal cortex by novel visual stimuli and a novel environment , 1997, Neuroscience Letters.

[216]  O. Smith,et al.  Afferent projections to the hypothalamic area controlling emotional responses (HACER) , 1982, Brain Research.

[217]  J. Isaac,et al.  Long-Term Depression of Kainate Receptor-Mediated Synaptic Transmission , 2006, Neuron.

[218]  R. Vertes,et al.  Projections of the median raphe nucleus in the rat , 1999, The Journal of comparative neurology.

[219]  Z. Bashir,et al.  Mechanisms and physiological role of enhancement of mGlu5 receptor function by group II mGlu receptor activation in rat perirhinal cortex , 2002, The Journal of physiology.

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

[221]  P Roullet,et al.  Nucleus accumbens dopamine receptors in the consolidation of spatial memory , 2004, Behavioural pharmacology.

[222]  M. W. Brown,et al.  Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain , 1995, Neuroscience.

[223]  G. Paxinos The Rat nervous system , 1985 .

[224]  M. Cassell,et al.  Cortical, thalamic, and amygdaloid projections of rat temporal cortex , 1997, The Journal of comparative neurology.

[225]  M. Fanselow,et al.  Amygdala Transcriptome and Cellular Mechanisms Underlying Stress-Enhanced Fear Learning in a Rat Model of Posttraumatic Stress Disorder , 2010, Neuropsychopharmacology.

[226]  Sean Commins,et al.  Massed but not spaced training impairs spatial memory , 2003, Behavioural Brain Research.

[227]  Z. Xiong,et al.  Differential Roles of NR2A- and NR2B-Containing NMDA Receptors in Activity-Dependent Brain-Derived Neurotrophic Factor Gene Regulation and Limbic Epileptogenesis , 2007, The Journal of Neuroscience.

[228]  M. Davis,et al.  Elicitation and reduction of fear: behavioural and neuroendocrine indices and brain induction of the immediate-early gene c-fos , 1997, Neuroscience.

[229]  R. Malach,et al.  Patterns of sensory intermodality relationships in the cerebral cortex of the rat , 1991, The Journal of comparative neurology.

[230]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[231]  Benjamin D. Philpot,et al.  Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity , 2008, Neuropharmacology.

[232]  Markus Wöhr,et al.  Playback of 22-kHz and 50-kHz ultrasonic vocalizations induces differential c-fos expression in rat brain , 2008, Neuroscience Letters.

[233]  A. Mele,et al.  Involvement of glutamatergic and dopaminergic systems in the reactivity of mice to spatial and non-spatial change , 1996, Psychopharmacology.

[234]  Joseph E LeDoux,et al.  Cells in the posterior thalamus project to both amygdala and temporal cortex: A quantitative retrograde double‐labeling study in the rat , 2000, The Journal of comparative neurology.

[235]  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.

[236]  E. Barkai,et al.  Cellular Correlates of Olfactory Learning in the Rat Piriform Cortex , 2001, Reviews in the neurosciences.

[237]  F. Artigas,et al.  Role of 5‐HT1A autoreceptors in the mechanism of action of serotoninergic antidepressant drugs: recent findings from in vivo microdialysis studies , 1996, Fundamental & clinical pharmacology.

[238]  R. Vertes,et al.  Ascending projections of the posterior nucleus of the hypothalamus: PHA‐L analysis in the rat , 1995, The Journal of comparative neurology.

[239]  D. Amaral,et al.  Entorhinal cortex of the rat: Topographic organization of the cells of origin of the perforant path projection to the dentate gyrus , 1998, The Journal of comparative neurology.

[240]  M. Gallagher,et al.  Alterations in [3H]‐kainate receptor binding in the hippocampal formation of aged long‐evans rats , 1993, Hippocampus.

[241]  Gareth R I Barker,et al.  Critical role of the cholinergic system for object-in-place associative recognition memory. , 2009, Learning & memory.

[242]  Rosemary A. Cowell,et al.  Paradoxical False Memory for Objects After Brain Damage , 2010, Science.

[243]  M. Eacott,et al.  Dissociable effects of lesions to the perirhinal cortex and the postrhinal cortex on memory for context and objects in rats. , 2005, Behavioral neuroscience.

[244]  S. S. Winans,et al.  The differential projections of the olfactory bulb and accessory olfactory bulb in mammals , 1975, The Journal of comparative neurology.

[245]  Tanemichi Chiba,et al.  Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study , 1991, Brain Research.

[246]  M. W. Brown,et al.  An experimental test of the role of postsynaptic calcium levels in determining synaptic strength using perirhinal cortex of rat , 2001, The Journal of physiology.

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

[248]  John P Aggleton,et al.  Lesions of the Rat Perirhinal Cortex Spare the Acquisition of a Complex Configural Visual Discrimination Yet Impair Object Recognition , 2010, Behavioral neuroscience.

[249]  A. Ylinen,et al.  Reciprocal Connections between the Amygdala and the Hippocampal Formation, Perirhinal Cortex, and Postrhinal Cortex in Rat: A Review , 2000, Annals of the New York Academy of Sciences.

[250]  H Eichenbaum,et al.  Neural Correlates of Olfactory Recognition Memory in the Rat Orbitofrontal Cortex , 2000, The Journal of Neuroscience.

[251]  R. Clark,et al.  An animal model of recognition memory and medial temporal lobe amnesia: History and current issues , 2010, Neuropsychologia.

[252]  X. Tong,et al.  GABA neurons provide a rich input to microvessels but not nitric oxide neurons in the rat cerebral cortex: A means for direct regulation of local cerebral blood flow , 2000, The Journal of comparative neurology.

[253]  T. Myhrer,et al.  Marked Retrograde and Anterograde Amnesia of a Visual Discrimination Task in Rats with Selective Lesions of the Perirhinal Cortex , 1996, Neurobiology of Learning and Memory.

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

[255]  T. Bussey,et al.  Transient Inactivation of Perirhinal Cortex Disrupts Encoding, Retrieval, and Consolidation of Object Recognition Memory , 2005, The Journal of Neuroscience.

[256]  M. Witter,et al.  Parallel input to the hippocampal memory system through peri‐ and postrhinal cortices , 1997, Neuroreport.

[257]  D. Bucci,et al.  Contextual fear discrimination is impaired by damage to the postrhinal or perirhinal cortex. , 2002, Behavioral neuroscience.

[258]  T. H. Brown,et al.  Three classes of pyramidal neurons in layer V of rat perirhinal cortex , 2002, Hippocampus.

[259]  Madeline J. Eacott,et al.  Recollection of episodic memory within the medial temporal lobe: Behavioural dissociations from other types of memory , 2010, Behavioural Brain Research.

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

[261]  J. Aggleton,et al.  The effects of neurotoxic lesions of the perirhinal cortex combined to fornix transection on object recognition memory in the rat , 1997, Behavioural Brain Research.

[262]  Joseph P. Huston,et al.  The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents , 2007, Neuroscience & Biobehavioral Reviews.

[263]  Z. Bashir,et al.  Differences in GABAergic transmission between two inputs into the perirhinal cortex , 2002, The European journal of neuroscience.

[264]  Joseph E LeDoux,et al.  Equipotentiality of thalamo-amygdala and thalamo-cortico-amygdala circuits in auditory fear conditioning , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[265]  H. Eichenbaum,et al.  Memory Representation within the Parahippocampal Region , 1997, The Journal of Neuroscience.

[266]  M. Avoli,et al.  Electrophysiology of regular firing cells in the rat perirhinal cortex , 2001, Hippocampus.

[267]  David Lodge,et al.  Differential roles of NR2A and NR2B-containing NMDA receptors in LTP and LTD in the CA1 region of two-week old rat hippocampus , 2007, Neuropharmacology.

[268]  P. Levitt,et al.  Regional Differences in Neurotrophin Availability Regulate Selective Expression of VGF in the Developing Limbic Cortex , 2001, The Journal of Neuroscience.

[269]  K. J. Canning,et al.  Lateral entorhinal, perirhinal, and amygdala‐entorhinal transition projections to hippocampal CA1 and dentate gyrus in the rat: A current source density study , 1998, Hippocampus.

[270]  Thomas M. Sanderson,et al.  Tyrosine Phosphatases Regulate AMPA Receptor Trafficking during Metabotropic Glutamate Receptor-Mediated Long-Term Depression , 2006, The Journal of Neuroscience.

[271]  D. S. Zahm,et al.  The patterns of afferent innervation of the core and shell in the “Accumbens” part of the rat ventral striatum: Immunohistochemical detection of retrogradely transported fluoro‐gold , 1993, The Journal of comparative neurology.

[272]  M W Brown,et al.  Fos imaging reveals differential neuronal activation of areas of rat temporal cortex by novel and familiar sounds , 2001, The European journal of neuroscience.

[273]  P. Liu,et al.  The effect of excitotoxic lesions centered on the hippocampus or perirhinal cortex in object recognition and spatial memory tasks. , 2001, Behavioral neuroscience.

[274]  Spartaco Santi,et al.  Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[275]  M. Witter,et al.  Significance of the deep layers of entorhinal cortex for transfer of both perirhinal and amygdala inputs to the hippocampus , 2008, Neuroscience Research.

[276]  T. Bussey,et al.  Distinct patterns of behavioural impairments resulting from fornix transection or neurotoxic lesions of the perirhinal and postrhinal cortices in the rat , 2000, Behavioural Brain Research.

[277]  M. Witter,et al.  Amygdala input promotes spread of excitatory neural activity from perirhinal cortex to the entorhinal-hippocampal circuit. , 2003, Journal of neurophysiology.

[278]  Ravi S. Menon,et al.  Novelty responses to relational and non‐relational information in the hippocampus and the parahippocampal region: A comparison based on event‐related fMRI , 2005, Hippocampus.

[279]  S. J. Shammah-Lagnado,et al.  Efferent connections of the nucleus of the lateral olfactory tract in the rat , 2004, The Journal of comparative neurology.

[280]  D. Overstreet,et al.  The flinders sensitive line rats, a genetic model of depression, show abnormal serotonin receptor mRNA expression in the brain that is reversed by 17beta-estradiol. , 1999, Brain research. Molecular brain research.

[281]  M. Witter,et al.  Entorhinal cortex of the rat: Cytoarchitectonic subdivisions and the origin and distribution of cortical efferents , 1998, Hippocampus.

[282]  G. Barker,et al.  Recognition Memory for Objects, Place, and Temporal Order: A Disconnection Analysis of the Role of the Medial Prefrontal Cortex and Perirhinal Cortex , 2007, The Journal of Neuroscience.

[283]  Alexander M. Benison,et al.  Auditory, somatosensory, and multisensory insular cortex in the rat. , 2008, Cerebral cortex.

[284]  G. V. Goddard,et al.  Development of Epileptic Seizures through Brain Stimulation at Low Intensity , 1967, Nature.

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

[286]  D. Mumby,et al.  Perirhinal cortex damage and anterograde object-recognition in rats after long retention intervals , 2007, Behavioural Brain Research.

[287]  R. Roth,et al.  The NMDA glycine site antagonist (+)-HA-966 selectively regulates conditioned stress-induced metabolic activation of the mesoprefrontal cortical dopamine but not serotonin systems: a behavioral, neuroendocrine, and neurochemical study in the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[288]  W. Löscher,et al.  Effects of lesions of the perirhinal cortex on amygdala kindling in rats , 2000, Epilepsy Research.

[289]  O. Phillipson,et al.  Afferent projections to the dorsal thalamus of the rat as shown by retrograde lectin transport. II. The midline nuclei , 1988, Brain Research Bulletin.

[290]  N. Tamamaki,et al.  Preservation of topography in the connections between the subiculum, field CA1, and the entorhinal cortex in rats , 1995, The Journal of comparative neurology.

[291]  R. Vertes A PHA‐L analysis of ascending projections of the dorsal raphe nucleus in the rat , 1991, The Journal of comparative neurology.

[292]  J. Michael Wyass,et al.  Connections between the retrosplenial cortex and the hippocampal formation in the rat: A review , 1992, Hippocampus.

[293]  F. Martı́nez-Soriano,et al.  Cytoarchitecture and efferent projections of the nucleus incertus of the rat , 2003, The Journal of comparative neurology.

[294]  E. Grove Efferent connections of the substantia innominata in the rat , 1988, The Journal of comparative neurology.

[295]  Miguel Remondes,et al.  Molecular mechanisms contributing to long-lasting synaptic plasticity at the temporoammonic-CA1 synapse. , 2003, Learning & memory.

[296]  D. Bilkey,et al.  Long‐term potentiation in the perirhinal‐hippocampal pathway is NMDA dependent , 1996, Neuroreport.

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

[298]  M. Cassell,et al.  Perirhinal cortex projections to the amygdaloid complex and hippocampal formation in the rat , 1999, The Journal of comparative neurology.

[299]  D. Paré,et al.  Low-probability transmission of neocortical and entorhinal impulses through the perirhinal cortex. , 2004, Journal of neurophysiology.

[300]  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.

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

[302]  P. Ernfors,et al.  Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for members of the trk family in the rat central nervous system , 1992, Neuroscience.

[303]  Chris J. Tinsley,et al.  Interfering with perirhinal brain‐derived neurotrophic factor expression impairs recognition memory in rats , 2011, Hippocampus.

[304]  S. Commins,et al.  Antagonism of glutamate receptors in the CA1 to perirhinal cortex projection prevents long-term potentiation and attenuates levels of brain-derived neurotrophic factor , 2009, Brain Research.

[305]  Toshio Iijima,et al.  Dual Transneuronal Tracing in the Rat Entorhinal-Hippocampal Circuit by Intracerebral Injection of Recombinant Rabies Virus Vectors , 2008, Front. Neuroanat..

[306]  T. Bussey,et al.  Perirhinal cortex and place-object conditional learning in the rat. , 2001, Behavioral neuroscience.

[307]  C. Saper,et al.  Convergence of autonomic and limbic connections in the insular cortex of the rat , 1982, The Journal of comparative neurology.

[308]  H. Carrer Mesencephalic participation in the control of sexual behavior in the female rat. , 1978, Journal of comparative and physiological psychology.

[309]  M. Witter,et al.  Projections from the parahippocampal region to the prefrontal cortex in the rat: evidence of multiple pathways , 2002, The European journal of neuroscience.

[310]  Z. Bashir,et al.  Cooperation between mglu receptors: a depressing mechanism? , 2002, Trends in Neurosciences.

[311]  S. Moses,et al.  Relational memory for object identity and spatial location in rats with lesions of perirhinal cortex, amygdala and hippocampus , 2005, Brain Research Bulletin.

[312]  M. Eacott,et al.  On familiarity and recall of events by rats , 2007, Hippocampus.

[313]  LTP in the rat basal amygdala induced by perirhinal cortex stimulation in vivo , 2000, Neuroreport.

[314]  M. Witter,et al.  Perirhinal cortex input to the hippocampus in the rat: evidence for parallel pathways, both direct and indirect. A combined physiological and anatomical study , 1999, The European journal of neuroscience.

[315]  J. Pearce,et al.  Novel temporal configurations of stimuli produce discrete changes in immediate‐early gene expression in the rat hippocampus , 2006, The European journal of neuroscience.

[316]  F. H. Lopes da Silva,et al.  Electrophysiological characterization of interlaminar entorhinal connections: an essential link for re‐entrance in the hippocampal–entorhinal system , 2003, The European journal of neuroscience.

[317]  Kara L. Agster,et al.  Functional neuroanatomy of the parahippocampal region in the rat: The perirhinal and postrhinal cortices , 2007, Hippocampus.

[318]  L. Saksida,et al.  Muscimol, AP5, or scopolamine infused into perirhinal cortex impairs two-choice visual discrimination learning in rats , 2010, Neurobiology of Learning and Memory.

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

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

[321]  A. Usiello,et al.  N-Methyl-D-aspartate receptors in the nucleus accumbens⋅are involved in detection of spatial novelty in mice , 1998, Psychopharmacology.

[322]  Rebecca D Burwell,et al.  Corticohippocampal Contributions to Spatial and Contextual Learning , 2004, The Journal of Neuroscience.

[323]  Asla Pitkänen,et al.  Projections from the posterior cortical nucleus of the amygdala to the hippocampal formation and parahippocampal region in rat , 2002, Hippocampus.

[324]  C. Beltramino,et al.  Dual action of electrochemical stimulation of the bed nucleus of the stria terminalis on the release of LH. , 1980, Neuroendocrinology.

[325]  D. Gaffan,et al.  A comparison of the effects of fornix transection and sulcus principalis ablation upon spatial learning by monkeys , 1989, Behavioural Brain Research.

[326]  A. McDonald,et al.  Amygdaloid connections with posterior insular and temporal cortical areas in the rat , 1987, The Journal of comparative neurology.

[327]  W. Krieg Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas , 1946 .

[328]  G. Biella,et al.  A fast transient outward current in layer II/III neurons of rat perirhinal cortex , 2007, Pflügers Archiv - European Journal of Physiology.

[329]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[330]  J. Price,et al.  Projections from the amygdala to the perirhinal and entorhinal cortices and the subiculum. , 1974, Brain research.

[331]  M. Witter,et al.  Anatomical Organization of the Parahippocampal‐Hippocampal Network , 2000, Annals of the New York Academy of Sciences.

[332]  C. Altar,et al.  Recombinant human nerve growth factor is biologically active and labels novel high-affinity binding sites in rat brain. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[333]  D. Amaral,et al.  Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat , 1998 .

[334]  J. Michael Wyss,et al.  Efferent connections of the anteromedial nucleus of the thalamus of the rat , 1999, Brain Research Reviews.

[335]  M. Mishkin,et al.  Neither perirhinal/entorhinal nor hippocampal lesions impair short-term auditory recognition memory in dogs , 2001, Neuroscience.

[336]  M. W. Brown,et al.  Changes in neuronal activity related to the repetition and relative familiarity of visual stimuli in rhinal and adjacent cortex of the anaesthetised rat , 1995, Brain Research.

[337]  S. Nakanishi,et al.  Distributions of the mRNAs for L‐2‐amino‐4‐phosphonobutyrate‐sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain , 1995, The Journal of comparative neurology.

[338]  T. van Groen,et al.  Extrinsic projections from area CA1 of the rat hippocampus: Olfactory, cortical, subcortical, and bilateral hippocampal formation projections , 1990, The Journal of comparative neurology.

[339]  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.

[340]  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.

[341]  G. Collingridge,et al.  Differential Roles of NR2A and NR2B-Containing NMDA Receptors in Cortical Long-Term Potentiation and Long-Term Depression , 2004, The Journal of Neuroscience.

[342]  Kara L. Agster,et al.  Cortical efferents of the perirhinal, postrhinal, and entorhinal cortices of the rat , 2009, Hippocampus.

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

[344]  R G Phillips,et al.  Contributions of postrhinal and perirhinal cortex to contextual information processing. , 2000, Behavioral neuroscience.

[345]  Boyer D. Winters,et al.  Object recognition memory: Neurobiological mechanisms of encoding, consolidation and retrieval , 2008, Neuroscience & Biobehavioral Reviews.

[346]  F. Gonzalez-Lima,et al.  Brain activity associated with fear renewal , 2006, The European journal of neuroscience.

[347]  Natalie L. M. Cappaert,et al.  The anatomy of memory: an interactive overview of the parahippocampal–hippocampal network , 2009, Nature Reviews Neuroscience.

[348]  M P Witter,et al.  Projections from the nucleus reuniens thalami to the entorhinal cortex, hippocampal field CA1, and the subiculum in the rat arise from different populations of neurons , 1996, The Journal of comparative neurology.

[349]  D. Bilkey,et al.  The effects of perirhinal cortical lesions on spatial reference memory in the rat , 1994, Behavioural Brain Research.

[350]  K. Fuxe,et al.  Cellular localization and distribution of dopamine D4 receptors in the rat cerebral cortex and their relationship with the cortical dopaminergic and noradrenergic nerve terminal networks , 2008, Neuroscience.

[351]  C Bucherelli,et al.  Auditory Thalamus, Dorsal Hippocampus, Basolateral Amygdala, and Perirhinal Cortex Role in the Consolidation of Conditioned Freezing to Context and to Acoustic Conditioned Stimulus in the Rat , 1999, The Journal of Neuroscience.

[352]  L. Saksida,et al.  Memory, perception, and the ventral visual‐perirhinal‐hippocampal stream: Thinking outside of the boxes , 2007, Hippocampus.

[353]  T. H. Brown,et al.  Fear conditioning to discontinuous auditory cues requires perirhinal cortical function. , 2008, Behavioral neuroscience.

[354]  C. Köhler Intrinsic connections of the retrohippocampal region in the rat brain: III. The lateral entorhinal area , 1988, The Journal of comparative neurology.

[355]  W. Staines,et al.  Efferent projections of the anterior perirhinal cortex in the rat , 1996, The Journal of comparative neurology.

[356]  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.

[357]  R. Vertes,et al.  Efferent projections of reuniens and rhomboid nuclei of the thalamus in the rat , 2006, The Journal of comparative neurology.

[358]  K. Murphy,et al.  Abnormal cortical synaptic plasticity in a mouse model of Huntington's disease , 2007, Brain Research Bulletin.

[359]  R G Phillips,et al.  Lesions of the fornix but not the entorhinal or perirhinal cortex interfere with contextual fear conditioning , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[360]  T. Bussey,et al.  Functionally Dissociating Aspects of Event Memory: the Effects of Combined Perirhinal and Postrhinal Cortex Lesions on Object and Place Memory in the Rat , 1999, The Journal of Neuroscience.

[361]  G. Barker,et al.  NMDA Receptor Plasticity in the Perirhinal and Prefrontal Cortices Is Crucial for the Acquisition of Long-Term Object-in-Place Associative Memory , 2008, The Journal of Neuroscience.

[362]  L. Savage,et al.  Memory for reward location is enhanced even though acetylcholine efflux within the amygdala is impaired in rats with damage to the diencephalon produced by thiamine deficiency , 2010, Neurobiology of Learning and Memory.

[363]  W. Krieg Connections of the cerebral cortex I. The Albino Rat. C. Extrinsic connections , 1947 .

[364]  F. Kloosterman,et al.  Physiology of the Entorhinal and Perirhinal Projections to the Hippocampus Studied by Current Source Density Analysis , 2000, Annals of the New York Academy of Sciences.

[365]  Piergiorgio Strata,et al.  Reversible inactivation of amygdala and cerebellum but not perirhinal cortex impairs reactivated fear memories , 2007, The European journal of neuroscience.

[366]  D. Bilkey,et al.  Instability in the Place Field Location of Hippocampal Place Cells after Lesions Centered on the Perirhinal Cortex , 2001, The Journal of Neuroscience.

[367]  O. Ottersen,et al.  Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase , 1982, The Journal of comparative neurology.

[368]  F. Gallyas,et al.  Activation of metabotropic glutamate receptors does not alter the phosphorylation state of GluR1 AMPA receptor subunit at serine 845 in perirhinal cortical neurons , 2004, Neuroscience Letters.

[369]  D. Mumby,et al.  Anterograde and retrograde memory for object discriminations and places in rats with perirhinal cortex lesions , 2000, Behavioural Brain Research.

[370]  G. Alheid,et al.  CHAPTER 19 – Amygdala and Extended Amygdala of the Rat: A Cytoarchitectonical, Fibroarchitectonical, and Chemoarchitectonical Survey , 2004 .

[371]  M. Roger,et al.  Ventral temporal cortex in the rat: Connections of secondary auditory areas Te2 and Te3 , 1990, The Journal of comparative neurology.

[372]  Jason J. Corneveaux,et al.  Tonic Premarin dose-dependently enhances memory, affects neurotrophin protein levels and alters gene expression in middle-aged rats , 2011, Neurobiology of Aging.

[373]  J M Wyss,et al.  An autoradiographic study of the efferent connections of the entorhinal cortex in the rat , 1981, The Journal of comparative neurology.

[374]  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.

[375]  L. Haberly,et al.  Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. , 2001, Chemical senses.

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

[377]  Rosemary A. Cowell,et al.  Components of recognition memory: Dissociable cognitive processes or just differences in representational complexity? , 2010, Hippocampus.

[378]  Changjun Shi,et al.  Visual Pathways Involved in Fear Conditioning Measured with Fear-Potentiated Startle: Behavioral and Anatomic Studies , 2001, The Journal of Neuroscience.

[379]  Gerardo Biella,et al.  Resurgent Na+ current in pyramidal neurones of rat perirhinal cortex: axonal location of channels and contribution to depolarizing drive during repetitive firing , 2007, The Journal of physiology.

[380]  W. Bai,et al.  Chemically defined feedback connections from infragranular layers of sensory association cortices in the rat , 2004, Neuroscience.

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

[382]  K. Kashihara,et al.  Regional Increases in Brain‐Derived Neurotrophic Factor and Nerve Growth Factor mRNAs During Amygdaloid Kindling, But Not in Acidic and Basic Fibroblast Growth Factor mRNAs , 1996, Epilepsia.

[383]  R. Maj,et al.  Brain-derived neurotrophic factor immunoreactivity in the limbic system of rats after acute seizures and during spontaneous convulsions: temporal evolution of changes as compared to neuropeptide Y , 1999, Neuroscience.

[384]  B. Woodside,et al.  Differential fos expression following aspiration, electrolytic, or excitotoxic lesions of the perirhinal cortex in rats. , 2005, Behavioral neuroscience.

[385]  Tim Otto,et al.  Behavioral and neuropsychological foundations of olfactory fear conditioning , 2000, Behavioural Brain Research.

[386]  R. Simerly,et al.  CHAPTER 14 – Anatomical Substrates of Hypothalamic Integration , 2004 .

[387]  Joseph E LeDoux,et al.  Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: contributions of contextual cues. , 1995, Behavioral neuroscience.

[388]  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.

[389]  N. Tamamaki,et al.  Projection of the entorhinal layer II neurons in the rat as revealed by intracellular pressure‐injection of neurobiotin , 1993, Hippocampus.

[390]  K. Hashimoto,et al.  d-Serine and a glycine transporter inhibitor improve MK-801-induced cognitive deficits in a novel object recognition test in rats , 2008, Behavioural Brain Research.

[391]  Peter Redgrave,et al.  Basal Ganglia , 2020, Encyclopedia of Autism Spectrum Disorders.

[392]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain , 1995, Hippocampus.

[393]  Mohamed T. Ghorbel,et al.  Expression of Long-Term Depression Underlies Visual Recognition Memory , 2008, Neuron.

[394]  S. O'dell,et al.  Impaired Object Recognition Memory Following Methamphetamine, but not p-Chloroamphetamine- or d-Amphetamine-Induced Neurotoxicity , 2005, Neuropsychopharmacology.

[395]  D. Bucci,et al.  BDNF expression in perirhinal cortex is associated with exercise-induced improvement in object recognition memory , 2010, Neurobiology of Learning and Memory.

[396]  F. Sargolini,et al.  NMDA and AMPA Antagonist Infusions into the Ventral Striatum Impair Different Steps of Spatial Information Processing in a Nonassociative Task in Mice , 2001, The Journal of Neuroscience.

[397]  H Eichenbaum,et al.  Afferent connections of the perirhinal cortex in the rat , 1983, The Journal of comparative neurology.

[398]  John F. Wesseling,et al.  Downregulation of NR3A-Containing NMDARs Is Required for Synapse Maturation and Memory Consolidation , 2009, Neuron.

[399]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[400]  J. Aggleton,et al.  Qualitatively different modes of perirhinal–hippocampal engagement when rats explore novel vs. familiar objects as revealed by c‐Fos imaging , 2010, The European journal of neuroscience.