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Author's Personal Copy 48 Anatomy of the Hippocampus and the Declarative Memory System CITATION: R. D. Burwell and K.Author's L. Agster. personal Anatomy of tcopyheHippocampus and the Declarative Memory System. In H. Eichenbaum (Ed.), Memory Systems. Vol. [3] of Learning and Memory: A Comprehensive Reference, 4 vols.(J.Byrne Editor), pp. [47-66] Oxford: Elsevier. 3.03 Anatomy of the Hippocampus and the Declarative Memory System R. D. Burwell and K. L. Agster, Brown University, Providence, RI, USA ª 2008 Elsevier Ltd. All rights reserved. 3.03.1 Introduction 47 3.03.1.1 A Short History of the Anatomy of Declarative Memory 47 3.03.1.2 Overview of the Hippocampal System 47 3.03.1.2.1 Nomenclature 47 3.03.1.2.2 Location of the hippocampal system structures 50 3.03.1.2.3 Cross-species comparisons: Human, monkey, and rodent 51 3.03.2 The Parahippocampal Region 52 3.03.2.1 The Postrhinal Cortex 52 3.03.2.2 The Perirhinal Cortex 53 3.03.2.3 Entorhinal Cortex 54 3.03.2.4 Presubiculum 57 3.03.2.5 The Parasubiculum 58 3.03.3 The Hippocampal Formation 58 3.03.3.1 The Dentate Gyrus 59 3.03.3.2 The Hippocampus Proper 61 3.03.3.3 The Subiculum 62 3.03.4 Conclusions 64 3.03.4.1 The Flow of Sensory Information through the Hippocampal System 64 3.03.4.2 The Comparative Anatomy of the Hippocampal System 65 References 65 3.03.1 Introduction functions? How do these structures interact to permit encoding, storage, consolidation, and retrieval 3.03.1.1 A Short History of the Anatomy of representations of facts and events? What of Declarative Memory additional cognitive functions might be supported? A half century ago, Scoville and Milner (1957) Understanding the structure and connectivity of described profound memory loss following bilateral these regions is necessary for generating and testing medial temporal lobe resection in the landmark sound hypotheses about the neurobiology of patient HM. In the following years, scientists study- memory. ing memory and the brain narrowed in on the hippocampus as the critical structure for everyday 3.03.1.2 Overview of the Hippocampal memory for facts and events. In the past two decades, System however, we have come full circle: It is now apparent that the cortical areas surrounding the hippocampal 3.03.1.2.1 Nomenclature formation also play critical roles in memory. Today, The structures that are the topic of this chapter have it is generally accepted that the hippocampal variously been termed the medial temporal lobe formation and the nearby parahippocampal region memory system (Squire and Zola-Morgan, 1991), together are necessary for human declarative mem- the hippocampal memory system (Eichenbaum ory, but many questions remain concerning the et al., 1994), and the hippocampal region (Witter functional diversity of structures within the so-called and Amaral, 2004). The terms hippocampal region declarative memory system. To what extent can the or hippocampal system have the advantage that the function of hippocampal and parahippocampal sub- terminology translates effectively from humans to structures be dissociated? How discrete are such animal models of human memory, including rodents. 47 Author's personal copy 48 Anatomy of the Hippocampus and the Declarative Memory System These regions are thought to support a type of mem- to the CA1. Finally, CA1 projects to the subiculum. ory that has been variously called episodic memory, Because corticocortical connections in the brain are declarative memory, or autobiographical memory. overwhelmingly reciprocal, such a multisynaptic, uni- For research on memory using animal models, the directional circuit is unique. In contrast, the entorhinal terms episodic or episodic-like memory may be most cortex projects to all portions of the hippocampal appropriate. formation. The connectivity and laminar structure of The hippocampal system comprises the hippocam- the entorhinal cortex differentiate it from hippocampal pal formation and the parahippocampal region formation structures. The dentate gyrus, hippocampus (Figure 1). The hippocampal formation includes the proper, and subiculum are therefore collectively dentate gyrus, the hippocampus proper (fields CA1, referred to as the hippocampal formation (Figure 3, CA2, and CA3), and the subiculum (Figure 2). The structures shown in yellow), and the entorhinal cortex primary criterion for inclusion in the hippocampal is considered part of the parahippocampal region. formation is the trilaminar character of the structures. The parahippocampal region, also called the In addition, the included structures are connected by retrohippocampal region, includes the perirhinal, largely unilateral pathways beginning with the dentate postrhinal (or parahippocampal), entorhinal, presu- gyrus granule cell input to the CA3 (Figure 3). CA3 bicular, and parasubicular cortices (Figure 1). The pyramidal cells, in turn, provide a unidirectional input postrhinal cortex in the rodent brain is considered the (a) (b)(c) D/S (d) Figure 1 Comparative views of the hippocampal system for the human (left), monkey (middle), and rat (right). The upper panel shows the relevant structures in lateral views of the human brain (a), the monkey brain (b), and the rodent brain (c). The lower panel shows unfolded maps of the relevant cortical structures for the human brain (d), the monkey brain (e), and the rodent brain (f). Shown for the human and monkey brain are unfolded layer IV maps of the perirhinal (PER) areas 35 and 36, parahippocampal (PH) areas TF and TH, and entorhinal cortex (EC). Figures adapted from Burwell RD, Witter MP, and Amaral DG (1995) The perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus 5: 390–408; Insausti R, Tun˜ o´ n T, Sobreviela T, Insausti AM, and Gonsalo LM (1995) The human entorhinal cortex: A cytoarchitectonic analysis. J. Comp. Neurol. 355: 171–198. Shown for the rodent brain are unfolded surface maps of the PER areas 35 and 36, the postrhinal cortex (POR), and the lateral and medial entorhinal areas (LEA and MEA). The rodent POR is the homolog of the primate PH (see text for details). In the monkey and the rat brain, the parasubiculum (ParaS) is interposed between the entorhinal and POR/PH (arrows). The pre- and parasubiculum, which are components of the parahippocampal region, are not shown (but see Figure 2). Abbreviations: cs, collateral sulcus; rs, rhinal sulcus; DG, dentate gyrus; D, dorsal; L, lateral; M, medial; ParaS,parasubiculum;PreS,presubiculum;S,septal;Sub,subiculum;T,temporal;V,ventral. Author's personal copy Anatomy of the Hippocampus and the Declarative Memory System 49 (a) (b) (c) Figure 2 Comparative views of the hippocampal formation with the pre- and parasubiculum. (a) Coronal sections of the human brain (a), monkey brain (b), and rat brain (c) showing the cellular layers of the hippocampal formation structures: the dentate gyrus (green), CA3 (blue), CA2 (purple), CA1 (red), and the subiculum (yellow). (d) An unfolded map of the rodent hippocampal formation. Rodent schematics adapted from Burwell RD and Witter MP (2002) Basic anatomy of the parahippocampal region in monkeys and rats. In: Witter MP and Wouterlood FG (eds.) The Parahippocampal Region, Organization and Role in Cognitive Functions. London: Oxford University Press. The presubiculum (light orange) and parasubiculum (dark orange) are also shown at two rostrocaudal levels in panels (e) and (f). Also shown are perirhinal areas 36 and 35 (panels (c) and (e)), the lateral and medial entorhinal areas (LEA and MEA, panels (e) and (f)), and the postrhinal cortex (POR, panel (f)). Abbreviations: DG, dentate gyrus; D, dorsal; L, lateral; M, medial; ParaS, parasubiculum; PreS, presubiculum; S, septal; Sub, subiculum; T, temporal; V, ventral. Author's personal copy 50 Anatomy of the Hippocampus and the Declarative Memory System There are also discrepancies in the terminology for the perirhinal cortex. In Brodmann’s (1909) nomenclature, which includes verbal and numeric terms, the verbal term for area 35 was perirhinal, and the verbal term for area 36 was ectorhinal. Although Brodmann defined area 36 as a very narrow strip of cortex that did not include the temporal pole, other classic studies, which reported more detailed cytoarchitectonic analyses of these regions, included the temporal pole in area 36 (von Economo, 1929; Von Bonin and Bailey, 1947). There was no designa- Figure 3 Simplified schematic of the hippocampal tion in Brodmann’s nomenclature for the caudally system. The schematic includes the hippocampal formation located region we now call the parahippocampal (structures in yellow) and the parahippocampal region (structures in red, blue, green, and orange). The cortex (reviewed in Suzuki and Amaral, 2003b). hippocampal formation comprises three-layered structures Using a different nomenclature, von Economo and characterized by largely unidirectional connections, Koskinsas named the rostral perirhinal/ectorhinal whereas the parahippocampal region comprises six- region areas TG and TGa and the caudal (parahip- layered cortices characterized by reciprocal connections. pocampal) region areas TF and TH. In modern Note that the perirhinal and postrhinal cortices (PER and POR) have reciprocal connections with CA1 and the terminology, the term perirhinal cortex was used to subiculum. Abbreviations: DG, dentate gyrus; EC, designate the combined areas 35 and 36 (Amaral entorhinal cortex; LEA, lateral entorhinal area; MEA, medial et al., 1987) or 35a and 35b (Van Hoesen and entorhinal area; ParaS, parasubiculum; PER, perirhinal Pandya, 1975). In the latter nomenclature, area 36 cortex; PH, parahippocampal cortex in the primate brain; was termed TL. POR, postrhinal cortex in the rodent brain; PreS, presubiculum; subiculum (SUB). Currently, the most commonly used nomencla- ture for memory research in the primate brain is perirhinal cortex comprising areas 35 and 36. Burwell and colleagues (Burwell et al., 1995; Burwell, 2001) adapted that nomenclature for use in homolog of the parahippocampal cortex in the primate the rodent brain. The term ectorhinal is no longer in brain.
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