Abstract
The hippocampus in mammals is a morphologically well-defined structure, and so are its main subdivisions. To define the homologous structure in other vertebrate clades, using these morphological criteria has been difficult, if not impossible, since the typical mammalian morphology is absent. Although there seems to be consensus that the most medial part of the pallium represents the hippocampus in all vertebrates, there is no consensus on whether all mammalian hippocampal subdivisions are present in the derivatives of the medial pallium in all vertebrate groups. The aim of this paper is to explore the potential relevance of connections to define the hippocampus across vertebrates, with a focus on mammals, reptiles, and birds.
References
1.
Abellan A, Desfilis E, Medina L (2014) Combinatorial expression of Lef1, Lhx2, Lhx5, Lhx9, Lmo3, Lmo4, and Prox1 helps to identify comparable subdivisions in the developing hippocampal formation of mouse and chicken. Front Neuroanat 8:59.
2.
Adamek GD, Shipley MT, Sanders MS (1984) The indusium griseum in the mouse: architecture, Timm's histochemistry and some afferent connections. Brain Res Bull 12:657-668.
3.
Aggleton JP (2014) Looking beyond the hippocampus: old and new neurological targets for understanding memory disorders. Proc Biol Sci 281:20140565.
4.
Aggleton JP, Christiansen K (2015) The subiculum: the heart of the extended hippocampal system. Prog Brain Res 219:65-82.
5.
Aggleton JP, McMackin D, Carpenter K, Hornak J, Kapur N, Halpin S, Wiles CM, Kamel H, Brennan P, Carton S, Gaffan D (2000) Differential cognitive effects of colloid cysts in the third ventricle that spare or compromise the fornix. Brain 123:800-815.
6.
Aggleton JP, O'Mara SM, Vann SD, Wright NF, Tsanov M, Erichsen JT (2010) Hippocampal-anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur J Neurosci 31:2292-2307.
7.
Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571-591.
8.
Andersen P, Bliss TV, Lomo T, Olsen LI, Skrede KK (1969) Lamellar organization of hippocampal excitatory pathways. Acta Physiol Scand 76:4A-5A.
9.
Annese J, Schenker-Ahmed NM, Bartsch H, Maechler P, Sheh C, Thomas N, Kayano J, Ghatan A, Bresler N, Frosch MP, Klaming R, Corkin S (2014) Postmortem examination of patient H.M.'s brain based on histological sectioning and digital 3D reconstruction. Nat Commun 5:3122.
10.
Augustinack JC, van der Kouwe AJ, Salat DH, Benner T, Stevens AA, Annese J, Fischl B, Frosch MP, Corkin S (2014) H.M.'s contributions to neuroscience: a review and autopsy studies. Hippocampus 24:1267-1286.
11.
Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331-356.
12.
Broca P (1878) Anatomie comparée des circonvolutions cérébrales. Le grand lobe limbique et la scissure limbique dans la série des mammifères. Rev Anthropol 2:285-498.
13.
Brun VH, Leutgeb S, Wu HQ, Schwarcz R, Witter MP, Moser EI, Moser MB (2008) Impaired spatial representation in CA1 after lesion of direct input from entorhinal cortex. Neuron 57:290-302.
14.
Brun VH, Otnass MK, Molden S, Steffenach HA, Witter MP, Moser MB, Moser EI (2002) Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296:2243-2246.
15.
Butler A (2017) Of horse-caterpillars and homologies: evolution of the hippocampus and its name. Brain Behav Evol 90:7-14.
16.
Eichenbaum H, Sauvage M, Fortin N, Komorowski R, Lipton P (2012) Towards a functional organization of episodic memory in the medial temporal lobe. Neurosci Biobehav Rev 36:1597-1608.
17.
Evensmoen HR, Ladstein J, Hansen TI, Moller JA, Witter MP, Nadel L, Haberg AK (2015) From details to large scale: the representation of environmental positions follows a granularity gradient along the human hippocampal and entorhinal anterior-posterior axis. Hippocampus 25:119-135.
18.
Evensmoen HR, Lehn H, Xu J, Witter MP, Nadel L, Haberg AK (2013) The anterior hippocampus supports a coarse, global environmental representation and the posterior hippocampus supports fine-grained, local environmental representations. J Cogn Neurosci 25:1908-1925.
19.
Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (2004) Spatial representation in the entorhinal cortex. Science 305:1258-1264.
20.
Hassiotis M, Paxinos G, Ashwell KW (2004) Cyto- and chemoarchitecture of the cerebral cortex of the Australian echidna (Tachyglossus aculeatus). I. Areal organization. J Comp Neurol 475:493-517.
21.
Haussler U, Rinas K, Kilias A, Egert U, Haas CA (2016) Mossy fiber sprouting and pyramidal cell dispersion in the hippocampal CA2 region in a mouse model of temporal lobe epilepsy. Hippocampus 26:577-588.
22.
Henriksen EJ, Colgin LL, Barnes CA, Witter MP, Moser MB, Moser EI (2010) Spatial representation along the proximodistal axis of CA1. Neuron 68:127-137.
23.
Hevner RF (2016) Evolution of the mammalian dentate gyrus. J Comp Neurol 524:578-594.
24.
Hoogland PV, Martinez-Garcia F, Vermeulen-Vanderzee E (1994) Are rostral and caudal parts of the hippocampus of the lizard Gekko gecko related to different types of behaviour? Eur J Morphol 32:275-278.
25.
Hoogland PV, Vermeulen-Vanderzee E (1995) Efferent connections of the lateral cortex of the lizard Gekko gecko: evidence for separate origins of medial and lateral pathways from the lateral cortex to the hypothalamus. J Comp Neurol 352:469-480.
26.
Insausti R, Herrero MT, Witter MP (1997) Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7:146-183.
27.
Kishi T, Tsumori T, Ono K, Yokota S, Ishino H, Yasui Y (2000) Topographical organization of projections from the subiculum to the hypothalamus in the rat. J Comp Neurol 419:205-222.
28.
Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser EI, Moser MB (2008) Finite scale of spatial representation in the hippocampus. Science 321:140-143.
29.
Knierim JJ, Neunuebel JP, Deshmukh SS (2014) Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and local-global reference frames. Philos Trans R Soc Lond B Biol Sci 369:20130369.
30.
Kohara K, Pignatelli M, Rivest AJ, Jung HY, Kitamura T, Suh J, Frank D, Kajikawa K, Mise N, Obata Y, Wickersham IR, Tonegawa S (2014) Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nat Neurosci 17:269-279.
31.
Kosel KC, Van Hoesen GW, Rosene DL (1982) Non-hippocampal cortical projections from the entorhinal cortex in the rat and rhesus monkey. Brain Res 244:201-213.
32.
Kropff E, Carmichael JE, Moser MB, Moser EI (2015) Speed cells in the medial entorhinal cortex. Nature 523:419-424.
33.
Kunzle H (2004) The hippocampal continuation (indusium griseum): its connectivity in the hedgehog tenrec and its status within the hippocampal formation of higher vertebrates. Anat Embryol (Berl) 208:183-213.
34.
Laplante F, Mnie-Filali O, Sullivan RM (2013) A neuroanatomical and neurochemical study of the indusium griseum and anterior hippocampal continuation: comparison with dentate gyrus. J Chem Neuroanat 50-51:39-47.
35.
Lewis FT (1923) The significance of the term hippocampus. J Comp Neurol 35:213-230.
36.
Lorente de Nó R (1933) Studies on the structure of the cerebral cortex. J Psychol Neurol 45:26-438.
37.
Lorente de Nó R (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol 46:113-177.
38.
Lu L, Igarashi KM, Witter MP, Moser EI, Moser MB (2015) Topography of place maps along the CA3-to-CA2 axis of the hippocampus. Neuron 87:1078-1092.
39.
Maass A, Berron D, Libby LA, Ranganath C, Duzel E (2015) Functional subregions of the human entorhinal cortex. Elife 4:e06426.
40.
Maclean PD (1952) Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalogr Clin Neurophysiol 4:407-418.
41.
Medina L, Abellan A, Desfilis E (2017) Contribution of genoarchitecture to understanding hippocampal evolution and development. Brain Behav Evol 90:25-40.
42.
Navarro Schroder T, Haak KV, Zaragoza Jimenez NI, Beckmann CF, Doeller CF (2015) Functional topography of the human entorhinal cortex. Elife 4:e06738.
43.
O'Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51:78-109.
44.
O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171-175.
45.
O'Keefe J, Nadel L (1978) The Hippocampus as a cognitive map. Oxford, Clarendon Press.
46.
Papez JW (1937) A proposed mechanism of emotion. Arch Neurol Psychiatry 38:725-743.
47.
Ramón y Cajal S (1893) Estructura del asta de Ammon y fascia dentata. Ann Soc Esp His Nat 22:53-114.
48.
Ramón y Cajal S (1902) Sobre un ganglio especial de la corteza esfeno-occipital. Trab Lab Invest Biol Univ Madrid 1:189-206.
49.
Ramón y Cajal S (1911) Histologie du système nerveux de l'homme et des vertébrés. Paris, Maloine.
50.
Ranganath C, Ritchey M (2012) Two cortical systems for memory-guided behaviour. Nat Rev Neurosci 13:713-726.
51.
Remondes M, Schuman EM (2004) Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 431:699-703.
52.
Rosene DL, Van Hoesen GW (1977) Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198:315-317.
53.
Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758-762.
54.
Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21.
55.
Smulders TV (2017) The avian hippocampal formation and the stress response. Brain Behav Evol 90:81-91.
56.
Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI (2008) Representation of geometric borders in the entorhinal cortex. Science 322:1865-1868.
57.
Sorensen KE (1985) The connections of the hippocampal region. New observations on efferent connections in the guinea pig, and their functional implications. Acta Neurol Scand 72:550-560.
58.
Squire LR, Wixted JT (2011) The cognitive neuroscience of human memory since H.M. Annu Rev Neurosci 34:259-288.
59.
Stephan H (1975) Allocortex. Berlin, Springer.
60.
Steward O (1976) Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 167:285-314.
61.
Strange BA, Witter MP, Lein ES, Moser EI (2014) Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci 15:655-669.
62.
Striedter GF (2016) Evolution of the hippocampus in reptiles and birds. J Comp Neurol 524:496-517.
63.
Swanson LW, Kohler C (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J Neurosci 6:3010-3023.
64.
Tamamaki N, Nojyo Y (1993) Projection of the entorhinal layer II neurons in the rat as revealed by intracellular pressure-injection of neurobiotin. Hippocampus 3:471-480.
65.
Treves A, Tashiro A, Witter ME, Moser EI (2008) What is the mammalian dentate gyrus good for? Neuroscience 154:1155-1172.
66.
Tsao A, Moser MB, Moser EI (2013) Traces of experience in the lateral entorhinal cortex. Curr Biol 23:399-405.
67.
Van der Werf YD, Jolles J, Witter MP, Uylings HB (2003a) Contributions of thalamic nuclei to declarative memory functioning. Cortex 39:1047-1062.
68.
Van der Werf YD, Scheltens P, Lindeboom J, Witter MP, Uylings HB, Jolles J (2003b) Deficits of memory, executive functioning and attention following infarction in the thalamus; a study of 22 cases with localised lesions. Neuropsychologia 41:1330-1344.
69.
Van Hoesen G, Pandya DN (1975a) Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents. Brain Res 95:1-24.
70.
Van Hoesen GW, Pandya DN (1975b) Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Res 95:39-59.
71.
Van Hoesen G, Pandya DN, Butters N (1975) Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents. Brain Res 95:25-38.
72.
van Strien NM, Cappaert NL, Witter MP (2009) The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 10:272-282.
73.
Willis T (1664) Cerebri anatome, cui accessit nervorum descripto et usus. Londini, typis Ja. Flesher, impensis Jo. Martyn & Ja. Allestry apud insigne Campanae in Coemeterio D. Pauli, p 538.
74.
Witter MP (2006) Connections of the subiculum of the rat: topography in relation to columnar and laminar organization. Behav Brain Res 174:251-264.
75.
Witter MP, Amaral DG (1991) Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex. J Comp Neurol 307:437-459.
76.
Witter MP, Griffioen AW, Jorritsma-Byham B, Krijnen JL (1988) Entorhinal projections to the hippocampal CA1 region in the rat: an underestimated pathway. Neurosci Lett 85:193-198.
77.
Witter MP, Groenewegen HJ (1986) Connections of the parahippocampal cortex in the cat. III. Cortical and thalamic efferents. J Comp Neurol 252:1-31.
78.
Witter MP, Groenewegen HJ (1990) The subiculum: cytoarchitectonically a simple structure, but hodologically complex. Prog Brain Res 83:47-58.
79.
Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33:161-253.
80.
Witter MP, Jorritsma-Byham B, Wouterlood FG (1992) Perforant pathway projections to the ammons horn and the subiculum in the rat. An electron microscopical PHAL study. Soc Neurosci Abstr 1:323.
81.
Witter MP, Naber PA, van Haeften T, Machielsen WC, Rombouts SA, Barkhof F, Scheltens P, Lopes da Silva FH (2000) Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10:398-410.
82.
Yeckel MF, Berger TW (1990) Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc Natl Acad Sci USA 87:5832-5836.
© 2017 S. Karger AG, Basel
2017
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.
