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The Rat Perirhinal Cortex: a Review of Anatomy, Physiology, Plasticity, and Function

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The Rat Perirhinal Cortex: a Review of Anatomy, Physiology, Plasticity, and Function View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by MURAL - Maynooth University Research Archive Library Progress in Neurobiology 93 (2011) 522–548 Contents lists available at ScienceDirect Progress in Neurobiology journal homepage: www.elsevier.com/locate/pneurobio The rat perirhinal cortex: A review of anatomy, physiology, plasticity, and function John Kealy, Sean Commins * Department of Psychology, National University of Ireland Maynooth, Maynooth, Co. Kildare, Ireland ARTICLE INFO ABSTRACT Article history: The perirhinal cortex is located in a pivotal position to influence the flow of information into and out of Received 19 April 2010 the hippocampal formation. In this review, we examine the anatomical, physiological and functional Received in revised form 28 January 2011 properties of the rat perirhinal cortex. Firstly, we review the properties of the perirhinal cortex itself, we Accepted 10 March 2011 describe how it can be separated into two distinct subregions and consider how it differs from other Available online 21 March 2011 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, Keywords: electrophysiological and plastic properties of its neurons. Secondly, we review the perirhinal cortex in Perirhinal cortex the context of its connections with other brain areas; focussing on the projections to cortical, subcortical Hippocampal formation Anatomy and hippocampal/parahippocampal regions. Particular attention is paid the anatomical and Physiology electrophysiological properties of these projections. Thirdly, we review the main functions of the Electrophysiology perirhinal cortex; its roles in perception, recognition memory, spatial and contextual memory and fear Perception conditioning are explored. Finally, we discuss the idea of anatomical, electrophysiological and functional Recognition memory segregation within the perirhinal cortex itself and as part of a hippocampal–parahippocampal network Spatial memory and suggest that understanding this segregation is of critical importance in understanding the role and Fear conditioning contributions made by the perirhinal cortex in general. ß 2011 Elsevier Ltd. All rights reserved. Contents 1. Introduction . 523 2. The perirhinal cortex . 523 2.1. Anatomical definition of the perirhinal cortex . 523 2.2. Neurotransmission in the perirhinal cortex. 525 2.3. Morphological and electrophysiological properties of perirhinal neurons . 525 2.4. Synaptic plasticity in the perirhinal cortex . 525 3. The perirhinal cortex and its projections . 526 3.1. Cortical projections. 526 3.2. Subcortical afferents and efferents of the perirhinal cortex . 529 3.3. Hippocampal and parahippocampal projections . 531 3.4. Anatomical and electrophysiological evidence for segregation within the hippocampal–parahippocampal network: the perirhinal cortex as part of this network . 534 3.5. Anatomical and electrophysiological evidence for segregation of function within the perirhinal cortex . 534 4. Function........................................................................................................ 535 4.1. Introduction . 535 4.2. The perirhinal cortex and perception. 536 4.3. Object recognition memory . 537 Abbreviations: AMPA, a-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate; BDNF, brain-derived neurotrophic factor; CA, Cornu Ammonis fields of hippocampus; CREB, cAMP response element-binding; D, dopamine receptor; fEPSP, field excitatory postsynaptic potential; GABA, g-aminobutyric acid; HFS, high frequency stimulation; 5-HT, serotonin receptor; LFS, low frequency stimulation; LTD, long-term depression; LTP, long-term potentiation; mGlu, metabotrophic glutamate receptor; MWM, Morris water maze; NGF, nerve growth factor; NMDA, N-methyl-D-aspartic acid; NR2, subunit of the NMDA receptor; NT, neurotrophin; PPD, paired-pulse depression; PPF, paired-pulse facilitation; Trk, tropomyosin-receptor-kinase. * Corresponding author. Tel.: +353 1 708 6182; fax: +353 1 708 4767. E-mail address: [email protected] (S. Commins). 0301-0082/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.pneurobio.2011.03.002 J. Kealy, S. Commins / Progress in Neurobiology 93 (2011) 522–548 523 4.4. The role of the perirhinal cortex in fear conditioning. 539 4.5. The role of the perirhinal cortex in context and spatial memory. 540 5. Implications of segregation and functionality . 541 6. Conclusions . 542 Acknowledgements . 542 References...................................................................................................... 542 1. Introduction sometimes protruding more rostrally than the dorsal subregion) and the posterior subregion is located caudally, bordering the The perirhinal cortex is considered along with the entorhinal postrhinal cortex. These three subregions are distinct from each and postrhinal cortices as an integral part of the parahippocampal other in that cells in layers II–V of the dorsal subregion are formation. It contributes both direct and indirect (via the organised radially whereas cells in the same layers of the ventral entorhinal cortex) projections to the hippocampus as well as subregion show no particular orientation and layers V and VI are being one of its main output structures. The perirhinal cortex is narrower in the dorsal subregion (Burwell and Amaral, 1998b; therefore pivotal in the processing of information into and out of Burwell, 2001). The posterior subregion differs from the rostral the hippocampal region. Although, there have been a number of subregions of area 36 due to the presence of round, medium-sized reviews that have specifically examined the anatomy (e.g. Burwell, cells throughout layers V and VI and the absence of a bilaminated 2001; van Strien et al., 2010) and functional roles of the perirhinal layer VI (Burwell, 2001). The borders of the perirhinal cortex with cortex (Dere et al., 2007; Winters et al., 2008; Warburton and the surrounding areas of neocortex can be determined in a similar Brown, 2010), to date, there has been no review that brings way to the divisions within the perirhinal cortex. The border with anatomy, physiology, synaptic plasticity and function of the posterior agranular insular cortex is located approximately 2.45– perirhinal cortex together. Here we attempt to bring these 2.80 mm posterior to the Bregma line and the two areas of cortex different strands together and also examine how the perirhinal differ in that the posterior agranular insular cortex has a trilaminar cortex fits within the general hippocampal–parahippocampal appearance and the presence of claustral cells but both these circuitry with particular emphasis on the electrophysiological features are absent in the perirhinal cortex (Burwell, 2001). The properties of these connections. visceral area has a granular layer IV making it distinct from the posterior agranular insular cortex but like the agranular insular 2. The perirhinal cortex cortex, the layers V and VI are distinct from each other. This is in contrast to the perirhinal cortex where the two layers are 2.1. Anatomical definition of the perirhinal cortex homogenous and is referred to as layer V (Burwell, 2001). The border with the ventral temporal association cortex is In the rat brain, the perirhinal cortex is located along the rhinal determinable by observing cell types in layer II; this layer of area sulcus and it is composed of Brodmann’s areas 35 and 36 (Brodmann, 36 of the perirhinal cortex is composed of round, medium-sized 1909), although later studies defined the perirhinal cortex as area 35 cells peppered with smaller pyramidal cells whereas a greater only (Krieg, 1946a). Area 36 occupies the dorsal bank of the rhinal number of cells in the ventral temporal association cortex are sulcus and area 35 occupies the ventral bank, extending slightly pyramidal in shape (Burwell, 2001). In addition, the ventral more rostrally than area 36 (Burwell, 2001). It is bordered rostrally temporal association cortex sometimes features layers either side by the posterior agranular insular cortex (bordering with areas 35 of layer V where cell density is lower but this feature is absent in and 36) and the visceral area (area 36 only), caudally by the the perirhinal cortex (Burwell, 2001). Layer VI in area 36 of the postrhinal cortex, dorsally by the ventral temporal association perirhinal cortex has a thick bilaminated appearance in contrast to cortex and ventrally by the lateral entorhinal cortex (Fig. 1a; Burwell both the ventral temporal association cortex and area 35 of the et al., 1995; Burwell, 2001; Paxinos and Watson, 2005). perirhinal cortex (Burwell, 2001). Finally, based on cortical input to The borders between the perirhinal cortex and its neighbouring either area, the perirhinal cortex receives markedly greater levels areas can be determined by cytoarchitectonic means, in particular of input from various cortical areas compared to the ventral the characteristic lack of a distinct layer IV in the perirhinal cortex temporal association area, i.e. the ventral temporal association (Burwell, 2001; Witter, 2002). Area 35 completely lacks layer IV area receives no input from the piriform but receives more while area 36 does have layer IV but it appears to be less well somatosensory and auditory input and lower levels of input from defined particularly in the medial portions of the cortex compared the insular
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