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Brain Structure and Function

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01.06.2004 | Original Article

The hippocampal continuation (indusium griseum): its connectivity in the hedgehog tenrec and its status within the hippocampal formation of higher vertebrates

verfasst von: H. Künzle

Erschienen in: Brain Structure and Function | Ausgabe 3/2004

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Abstract

The indusium griseum and its precallosal extension are usually considered poorly differentiated portions of the hippocampus. The connections of this so-called ‘hippocampal continuation’ (HCt) have only been analyzed so far in rodents, which show one of the least-developed HCt among mammals. In this study we have investigated the relatively well differentiated HCt of the small Madagascan hedgehog tenrec (Afrotheria) using histochemical and axonal transport techniques. The tenrec’s HCt shows associative and commissural connections. It receives laminar specific afferents from the entorhinal cortex (collaterals from neurons projecting to the dentate area), the anterior and posterior piriform cortices as well as the supramammillary region. A few fibers also originate in the olfactory bulb and the dentate hilus. Among these input areas only the dentate hilus receives a significant reciprocal projection from the HCt. Additional HCt efferents are directed to the subcallosal septum (presumed septohippocampal nucleus), the olfactory tubercle and the islands of Calleja. With the exception of the supramammillary afferents and possible efferents to the supraoptic nucleus we failed, however, to demonstrate distinct thalamic and hypothalamic connections. A comparison of the connections of the HCt with those of the hippocampal subdivisions reveal some similarity between the HCt and the dentate area, but the overall pattern of connectivity does not permit a correlation of the HCt with the dentate area, let alone the cornu ammonis and the subiculum. This view is supported by histochemical findings in the tenrec (immunoreactivity to calcium binding proteins) as well as the rat (data taken from the literature). The HCt is therefore considered a region in its own right within the hippocampal formation. It may be tentatively correlated with the medial cortex of reptiles, while the dentate area and the cornu ammonis may have evolved de novo in mammals.

The nomenclature used here restricts the term taenia tecta to the region reciprocally connected with the olfactory bulb (Radtke-Schuller and Künzle 2000). Showing a less compact layer 2 and a layer 3 with mainly medium-sized, round neurons; this region is also referred to as the ventral taenia tecta, while the HCtA is called the dorsal taenia tecta (Haberly and Price 1978).

Among the candidate regions (subicular complex, entorhinal cortex) often cited in this respect, the entorhinal cortex is considered here as part of the caudolateral hemisphere which might have evolved in parallel to the Dt and CA. This assumption is made on the basis of: (1) the similarity between the entorhinal cortex and the primary olfactory cortex with regard to their three-layered organization in tenrec (Künzle 2002); (2) the presence of reciprocal connections between the mammalian entorhinal cortex and both the primary olfactory cortex and the olfactory bulb (Amaral and Witter 1995; Haberly 2001). The latter regions are poorly connected with the areas laterally adjacent to the reptilian MDM (Ulinski 1990; Hoogland and VanderZee 1995).

Abbie AA (1939) The origin of the corpus callosum and the fate of structures related to it. J Comp Neurol 70:9–44

Aboitiz F, Montiel J, Morales D, Concha M (2002) Evolutionary divergence of the reptilian and the mammalian brains: considerations on connectivity and development. Brain Res Rev 39:141–153CrossRefPubMed

Adamek GD, Shipley MT, Sanders MS (1984) The indusium griseum in the mouse: architecture, Timm’s histochemistry and some afferent connections. Brain Res Bull 12:657–668CrossRefPubMed

Albright CD, Friedrich CB, Brown EC, Mar MH, Zeisel SH (1999) Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum. Dev Brain Res 115:123–129CrossRef

Allen GV, Hopkins DA (1989) Mamillary body in the rat: topography and synaptology of projections from the subicular complex, prefrontal cortex and midbrain tegmentum. J Comp Neurol 286:311–337PubMed

Amaral DG, Witter, MP (1995) Hippocampal formation. In: Paxinos G (ed) The Rat Nervous System, 2nd edn. Academic Press, San Diego pp 443–493

Atoji W, Wild JM, Yamamoto Y, Suzuki Y (2002) Intratelencephalic connections of the hippocampus in pigeons (Columba livia). J Comp Neurol 447:177–199CrossRefPubMed

Bekirov IH, Needleman LA, Zhang W, Benson DL (2002) Identification and localization of multiple classic cadherins in developing rat limbic system. Neuroscience 115:213–227CrossRefPubMed

Blasco-Ibanez JM, Freund TF (1997) Distribution, ultrastructure, and connectivity of calretinin-immunoreactive mossy cells of the mouse dentate gyrus. Hippocampus 7:307–320CrossRefPubMed

Blumenau L (1891) Zur Entwicklungsgeschichte und feineren Anatomie des Hirnbalkens. Archiv f mikrosk Anat 37:1–15

Bruce LL, Neary TJ (1995) Afferent projections to the lateral and dorsomedial hypothalamus in a lizard Gekko gecko. Brain Behav Evol 46:30–42PubMed

Butler AB, Hodos W (eds) (1996) Comparative Vertebrate Neuroanatomy. Evolution and Adaptation. Wiley, New York

Cassell MD, Brown MW (1984) The distribution of Timm’s stain in the nonsulphide-perfused human hippocampal formation. J Comp Neurol 222:461–471PubMed

Cassell MD, Wright DJ (1986) Topography of projections from the medial prefrontal cortex to the amygdala in the rat. Brain Res Bull 17:321–333CrossRefPubMed

Cavada C, Company T, Tejedor J, Cruz-Rizzolo RJ, Reinoso-Suarez F (2000) The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cerebral Cortex 10:220–242CrossRefPubMed

Celio MR (1990) Calbindin D-28 k and parvalbumin in the rat nervous system. Neuroscience 35:375–475PubMed

Charnay Y, Leger L, Vallet PG, Hof PR, Jouvet M, Bouras C (1995) (3H)Nisoxetine binding sites in the cat brain: an autoradiographic study. Neuroscience 69:259–270CrossRefPubMed

Chen S, Aston-Jones G (1998) Axonal collateral-collateral transport of tract tracers in brain neurons: false anterograde labelling and useful tool. Neuroscience 82:1151–1163CrossRefPubMed

Conde F, Mairelepoivre E, Audinat E, Crepel F (1995) Afferent connections of the medial frontal cortex of the rat. 2. Cortical and subcortical afferents. J Comp Neurol 352:567–593PubMed

Das GD (1971) Experimental studies on the postnatal development of the brain. I. Cytogenesis and morphogenesis of the accessory fascia dentata following hippocampal lesions. Brain Res 28:263–282CrossRefPubMed

Desan PH (1988) Organization of the cerebral cortex in turtle. In: Schwerdtfeger WK, Smeets WJAJ, (eds) The Forebrain of Reptiles. Karger, Basel pp 1–11

Douady CJ, Douzery EJP (2003) Molecular estimation of eulipotyphlan divergence times and the evolution of “Insectivora”. Mol Phylogen Evol 28:285–296CrossRef

Fallon JH, Loughlin SE, Ribak CE (1983) The islands of Calleja complex of rat basal forebrain. III. Histochemical evidence for a striatopallidal system. J Comp Neurol 218:91–120PubMed

Fernandez AS, Pieau C, Repérant J, Boncinelli E, Wassef M (1998) Expression of the Emx-1 and Dlx-1 homebox genes define three molecularly distinct domains in the telencephalon of mouse, chick, turtle and frog embryos: implications for the evolution of telencephalic subdivisions in amniotes. Development 125:2099–2111PubMed

Finch DM (1993) Hippocampal, subicular, and entorhinal afferents and synaptic integration in rodent cingulate cortex. In: Vogt B, Gabriel M, Gabriel M (eds) Neurobiology of Cingulate Cortex and Limbic Thalamus. Birkhäuser, Berlin, pp 224–248

Fish PA (1893) The indusium of the callosum. J Comp Neurol 3:61–68

Floyd NS, Price JL, Ferry AT, Keay KA, Bandler R (2001) Orbitomedial prefrontal cortical projections to hypothalamus in the rat. J Comp Neurol 432:307–328CrossRefPubMed

Flügge G, Schniewind A, Fuchs E (1988) The corticosterone receptive system in the brain of Tupaia belangeri visualized by in vivo autoradiography. Expl Brain Res 72:417–424

Font C, Martínez-Marcos A, Lanuza E, Hoogland PV, Martínez-Garcia F (1997) Septal complex of the telencephalon of the lizard Podarcis hispanica. J Comp Neurol 383:489–511CrossRefPubMed

Font C, Lanuza E, Martinez-Marcos A, Hoogland PV, Martinez-Garcia F (1998) Septal complex of the telencephalon of lizards: III. Efferent connections and general discussion. J Comp Neurol 401:525–548CrossRefPubMed

Gall CM, Berschauer R, Isackson PJ (1994) Seizures increase basic fibroblast growth factor mRNA in adult rat forebrain neurons and glia. Mol Brain Res 21:190–205CrossRefPubMed

Gaykema RPA, Lutten PGM, Nyakas C (1990) Cortical projection patterns of the medial septum-diagonal band complex. J Comp Neurol 293:103–125PubMed

Gloor P (ed) (1997) The Temporal Lobe and Limbic System. Oxford University Press, New York

Haberly LB (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26:551–576CrossRefPubMed

Haberly LB, Price, JL (1978) Association and commissural fiber systems of the olfactory cortex of the rat. II. Systems originating in the olfactory peduncle. J Comp Neurol 181:781–808PubMed

Haglund L, Swanson LW, Köhler C (1984) The projection of the supramammillary nucleus to the hippocampal formation: An immunohistochemical anterograde transport study with the lectin PHA-L in the rat. J Comp Neurol 229:171–185PubMed

Hamel EG (1982) Telencephalon of marsupials. In: Crosby E, Schnitzlein H, Schnitzlein H. (eds) Comparative Correlative Neuroanatomy of the Vertebrate Telencephalon. MacMillan, New York, pp 317–335

Higuchi T, Okere CO (2002) Role of the supraoptic nucleus in regulation of parturition and milk ejection revisited. Microsc Res Tech 56:113–121CrossRefPubMed

Hjorth-Simonsen A (1972) Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata. J Comp Neurol 146:219–232PubMed

Hoogland PV, Vermeulen-Vanderzee E (1989) Efferent connections of the dorsal cortex of the lizard Gekko gecko studied with Phaseolus vulgaris - leucoagglutinin. J Comp Neurol 285:289–303PubMed

Hoogland PV, Vermeulen-Vanderzee E (1993) Medial cortex of the lizard Gekko-gecko - a hodological study with emphasis on regional specialization. J Comp Neurol 331:326–338PubMed

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 352:469–480PubMed

Hori A, Peiffer J, Peiffer RA, Lizuka R (1980) Cerebello-cortical heterotopia in dentate nucleus, and other microdysgeneses in trisomy DI (Patau) syndrome. Brain Dev 2:345–352PubMed

Hurley KM, Herbert H, Moga MM, Saper CB (1991) Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308:249–277PubMed

Hyland BI, Sirett NE, Hubbard JI (1986) Electrophysiological evidence for a projection from medial pre-frontal and anterior limbic cortex toward the medial preoptic area in the cat. Exp Brain Res 63:205–215PubMed

Ino T, Yasui Y, Itoh K, Nomura S, Akiguchi T, Kameyama M, Mizuno N (1987) Direct projections from ammon’s horn to the septum in the cat. Exp Brain Res 68: 179–188PubMed

Irle E, Markowitsch HJ (1982) Connections of the hippocampal formation, mammillary bodies, anterior thalamus and cingulate cortex. Exp Brain Res 47:79–94PubMed

Ishizuka N (2001) Laminar organization of the pyramidal cell layer of the subiculum in the rat. J Comp Neurol 435:89–110PubMed

Ito A, Saito N, Hirata M, Kose A, Tsujino T, Yoshihara C, Ogita K, Kishimoto A, Nishizuka Y, Tanaka C (1990) Immunocytochemical localization of a subspecies of protein kinase C in rat brain. Proc Natl Acad Sci USA 87:3195–3199PubMed

Jay TM, Witter MP (1991) Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus-vulgaris-leucoagglutinin. J Comp Neurol 313:574–587PubMed

Johnston JB (1913) The morphology of the septum, hippocampus, and pallial commissures in reptiles and mammals. J Comp Neurol 23:371–478

Kloosterman F, Witter MP, van Haeften T (2003) Topographical and laminar organization of subicular projections to the parahippocampal region of the rat. J Comp Neurol 455:156–171CrossRefPubMed

Kuhlenbeck H (1977) Derivatives of the Prosencephalon: Diencephalon and Telencephalon. The Central Nervous System of Vertebrates, vol 5, part I. Karger, Basel, pp 1–888

Künzle H (1998) Thalamic territories innervated by cerebellar nuclear afferents in the hedgehog tenrec, Echinops telfairii. J Comp Neurol 402:313–326CrossRefPubMed

Künzle H (2002) Distribution of perihippocampo-hippocampal projection neurons in the lesser hedgehog tenrec. Neurosci Res 44:405–419CrossRefPubMed

Künzle H (2003) Neocortical connections with perihippocampal and periamygdalar regions in the hedgehog tenrec. Anat Embryol 207:389–407CrossRefPubMed

Künzle H, Rehkämper G (1992) Distribution of cortical neurons projecting to dorsal column nuclear complex and spinal cord in the hedgehog-tenrec, Echinops telfairi. Somatosens Mot Res 9:185–197PubMed

Künzle H, Radtke-Schuller S (2000) Basal telencephalic regions connected with the olfactory bulb in the Madagascan hedgehog tenrec. J Comp Neurol 423:706–726CrossRefPubMed

Künzle H, Radtke-Schuller S (2001) Hippocampal fields in the hedgehog tenrec. Their architecture and major intrinsic connections. Neurosci Res 41:267–291CrossRefPubMed

Künzle H, Radtke-Schuller S, von Stebut B (2002) Parabrachio-cortical connections with the lateral cerebral hemisphere in the Madagascan hedgehog tenrec: prominent projections to layer 1, weak projections from layer 6. Brain Res Bull 57:705–719CrossRefPubMed

Lanuza E, Halpern M (1998) Efferents and centrifugal afferents of the main and accessory olfactory bulbs in the snake Thamnophis sirtalis. Brain Behav Evol 51:1-22CrossRefPubMed

Li XG, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181–208PubMed

Lippa CF, Smith TW (1992) The indusium griseum in Alzheimer’s disease: an immunocytochemical study. J Neurol Sci 111:39–45CrossRefPubMed

Llewellyn-Smith IJ, Pilowsky P, Minson JB (1993) The tungstate-stabilized tetramethylbenzidine reaction for light and electron microscopic immunocytochemistry and for revealing biocytin-filled neurons. J Neurosci Meth 46:27–40CrossRef

Lohman AHM, van Woerden-Verkley I (1978). Ascending connections to the forebrain in the Tegu lizard. J Comp Neurol 182:555–574PubMed

Lohman AHM, Smeets WJAJ (1993) Overview of the main and accessory olfactory bulb projections in reptiles. Brain Behav Evol 41:147–155PubMed

Lopez-Garcia C, Martinez-Guijaro FJ, Berbel P, Garcia-Verdugo JM (1988). Long-spined polymorphic neurons of the medial cortex of lizards: a Golgi, Timm and electron-microscopic study. J Comp Neurol 272:409–423PubMed

Luskin MB, Price JL (1983) The laminar distribution of intracortical fibers originating in the olfactory cortex of the rat. J Comp Neurol 216:292–302PubMed

Martinez-Garcia F, Amiguet M, Olucha F, Lopez-Garcia C (1986) Connections of the lateral cortex in the lizard Podarcis hispanica. Neurosci Lett 63:39–44CrossRefPubMed

Martinez-Garcia F, Olucha FE (1988) Afferent projections to the Timm-positive cortical areas of the telencephalon of lizards. In: Schwerdtfeger W, Smeets WJAJ (eds) Recent advances in understanding the structure and function of the forebrain in reptiles. Karger, Basel, pp 30–40

Martinez-Guijarro FJ, Desfilis E, Lopez-Garcia C (1990) Organization of the dorsomedial cortex in the lizard Podarcis hispanica. Expl Brain Res 19:77–92

McIntyre DC, Kelly ME, Staines WA (1996) Efferent projections of the anterior perirhinal cortex in the rat. J Comp Neurol 369:302–318CrossRefPubMed

Merchenthaler I, Görcs T, Sétáló G (1982) Neurons containing luteinizing hormone-releasing hormone in the indusium griseum of the rat. Acta Morph Acad Sci Hung 30:151–156

Merchenthaler I, Görcs T, Sétáló P, Tetrusz P, Flerkó B (1984) Gonadotropin-releasing hormone (GnRH) neurons and pathways in the rat brain. Cell Tiss Res 237:15–29

Monaghan DT, Yao D, Cotman CW (1984) Distribution of (3H)AMPA binding sites in rat brain as determined by quantitative autoradiography. Brain Res 324:160–164CrossRefPubMed

Montagnese CM, Krebs JR, Meyer G (1996) The dorsomedial and dorsolateral forebrain of the zebra finch, Taeniopygia guttata: a Golgi study. Cell Tiss Res 283:263–282CrossRef

Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8:608–619CrossRefPubMed

Nakada T (1999) High-field, high-resolution MR imaging of the human indusium griseum. AJNR Am J Neuroradiol 20:524–525PubMed

Nambu T, Sakurai T, Sakurai T, Mizukami K, Hosoya Y, Yanagisawa M, Goto K (1999) Distribution of orexin neurons in the adult rat brain. Brain Res 827:243–260PubMed

Nikaido M, Cao Y, Okada N, Hasegaswa M (2003) The phylogenetic relationships of insectivores with special reference to the lesser hedgehog tenrec as inferred from the complete sequence of theri mitochondrial genome. Genes Genet Syst 78:107–112CrossRefPubMed

Obersteiner H (1888) Anleitung beim Studium des Baues der nervösen Centralorgane im gesunden und kranken Zustande. Toeplitz, Leipzig

Ohtake T, Yamada H (1989) Efferent connections of the nucleus reuniens and the rhomboid nucleus in the rat: an anterograde PHA-L tracing study. Neurosci Res 6:556–569CrossRefPubMed

Pasquier DA, Reinoso-Suarez F (1978) The topographic organization of hypothalamic and brain stem projections to the hippocampus. Brain Res Bull 3:373–389CrossRefPubMed

Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JLR (2000) Pallial and subpallial derivates in the embryonic chick and mouse telencephalon, traced by the expression of the genes DIx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409–438CrossRefPubMed

Rabhi M, Stoeckel ME, Calas A, Freund-Mercier MJ (1999) Historadioautographic localisation of oxytocin and vasopressin binding sites of the merione (Meriones shawi).Brain Res Bull 48:147–163CrossRefPubMed

Radtke-Schuller S, Künzle H (2000) Olfactory bulb and retrobulbar regions in the hedgehog tenrec. Their organization and interconnections. J Comp Neurol 423:687–705CrossRefPubMed

Reep RL, Goodwin GS, Corwin JV (1990) Topographic organization in the corticocortical connections of medial agranular cortex in rats. J Comp Neurol 294:262–281PubMed

Room P, Groenewegen HJ (1986) Connections of the parahippocampal cortex. I. Cortical afferents. J Comp Neurol 251:415–450PubMed

Room P, Russchen FT, Groenewegen HJ, Lohman AHM (1985) Efferent connections of the prelimbic (area 32) and the infralimbic (area 25) cortices: an anterograde tracing study in the cat. J Comp Neurol 242:40–55PubMed

Rose M (1926) Der Allocortex bei Tier und Mensch. J Psychol Neurol 34:1–99

Ruit KG, Neafsey EJ (1990) Hippocampal input to a “visceral motor” corticobulbar pathway: an anatomical and electrophysiological study in the rat. Exp Brain Res 82:606–616PubMed

Schmued LC, Bowyer JF (1997) Methamphetamine exposure can produce neuronal degeneration in mouse hippocampal remnants. Brain Res 759:135–140PubMed

Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213–242PubMed

Shibata H (1989) Descending projections to the mammillary nuclei in the rat, as studied by retrograde and anterograde transport of wheat germ agglutinin-horseradish peroxidase. J Comp Neurol 285:436–453PubMed

Shibata H (1993) Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J Comp Neurol 330:533–542PubMed

Shipley MT, Adamek GD (1984) The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res Bull 12:669–688PubMed

Shipley MT, Ennis M (1996) Functional organization of olfactory system. J Neurobiol 30:123–176CrossRefPubMed

Smith GE (1897) The morphology of the indusium and striae lancisii. Anat Anzeiger 13:23–27

Stephan H (1975) Allocortex. In: Bargmann W (ed) Handbuch der mikr. Anatomie des Menschen, vol 4, Teil 9. Springer, Berlin, Heidelberg, New York p 998

Stephan H, Baron G, Frahm HD (1991) Insectivora. Comp Brain Res Mammals vol 1. Springer, Berlin, Heidelberg, New York p 573

Stumpf WE, Heiss C, Sar M, Duncan GE, Craver C (1989) Dexamethasone and corticosterone receptor sites. Histochem 92:201–210

Sturrock RR (1978) Development of the indusium griseum. III. An autoradiographic study of cell production. J Anat 126:1–6PubMed

Swanson LW, Hartman BK (1975) The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-B-hydroxylase as a marker. J Comp Neurol 163:467–506PubMed

Swanson LW, Köhler C (1986) Anatomical evidence for direct projections from the entorhinal area to the entire cortical mantle in the rat. J Neurosci 6:3010–3023PubMed

Szekely AD (1999) The avian hippocampal formation: subdivisions and connectivity. Behav Brain Res 98:219–225CrossRefPubMed

Takagishi M, Chiba T (1991) Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study. Brain Res 566:26–39CrossRefPubMed

Tamamaki N, Nojyo Y (1995) Preservation of topography in the connections between the subiculum, field CA1, and the entorhinal cortex in rats. J Comp Neurol 353:379–390PubMed

Tilney F (1939) The hippocampus and its relations to the corpus callosum. J nerv ment Disease 89:433–513

Tömböl T, Davies DC, Németh A, Sebestény T (2000) A comparative Golgi study of chicken (Gallus domesticus) and homing pigeon (Columba livia) hippocampus. Anat Embryol 201:85–101PubMed

Tole S, Grove EA (2001) Detailed field pattern is intrinsic to the embryonic mouse hippocampus early in neurogenesis. J Neurosci 21:1580–1588PubMed

Travis NMG (1982) Telencephalon of an edentate. In: Crosby E, Schnitzlein H (eds), Comparative Correlative Neuroanatomy of the Vertebrate Telencephalon. MacMillan, New York, pp 338–373

Ulinski PS (1990) The cerebral cortex of reptiles. In: Jones EG, Peters A (eds) Cerebral Cortex, vol 8A. Plenum, New York pp 139–205

Van der Werf YD, Witter MP, Groenewegen HJ (2002) The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Rev 39:107–140CrossRefPubMed

Van Groen T, Wyss JM (1990) Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J Comp Neurol 302:515–528PubMed

Van Groen T, Kadish I, Wyss JM (1999) Efferent connections of the anteromedial nucleus of the thalamus of the rat. Brain Res Rev 30:1–26CrossRefPubMed

Van Hoesen GW, Mesulam MM, Haaxma R (1976) Temporal cortical projections to the olfactory tubercle in the rhesus monkey. Brain Res 109: 375–381CrossRefPubMed

Vertes RP (1992) PHA-L analysis of projections from the supramammillary nucleus in the rat. J Comp Neurol 326:595–622PubMed

Vertes RP (2002) Analysis of projections from the medial prefrontal cortex to the thalamus in the rat, with emphasis on nucleus reuniens. J Comp Neurol 442:163–187

Weaver DR, Deeds JD, Lee K, Segre GV (1995) Localization of parathyroid hormone-related peptide (PTHrP) and PTH/PTHrP receptor mRNAs in rat brain. Mol Brain Res 28:296–310CrossRefPubMed

Witter MP, Wouterlood FG, Naber PA, van Haeften T (2000) Anatomical organization of the parahippo-campal-hippocampal network. In: Scharfman H, Witter M, Schwarcz R (eds) The Parahippocampal Region, Implications for Neurological and Psychiatric Diseases. Ann NY Acad Sci 911:1–24PubMed

Woods WH, Holland RC, Powell EW (1969) Connections of cerebral structures functioning in neurohypophysial hormone release. Brain Res 12:26–46CrossRefPubMed

Wouterlood FG, Saldana E, Witter MP (1990) 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. J Comp Neurol 296:179–203PubMed

Wyss JM, Sripanidkulchai K (1983) The indusium griseum and anterior hippocampal continuation in the rat. J Comp Neurol 219:251–272PubMed

Yanagihara M, Niimi K, Ono K (1987) Thalamic projections to the hippocampal and entorhinal areas in the cat. J Comp Neurol 266:122–141PubMed

Zhao XY, Lein ES, He AQ, Smith SC, Aston C, Gage FH (2001) Transcriptional profiling reveals strict boundaries between hippocampal subregions. J Comp Neurol 441:187–196CrossRefPubMed

Titel: The hippocampal continuation (indusium griseum): its connectivity in the hedgehog tenrec and its status within the hippocampal formation of higher vertebrates
verfasst von: H. Künzle
Publikationsdatum: 01.06.2004
Verlag: Springer-Verlag
Erschienen in: Brain Structure and Function / Ausgabe 3/2004
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-004-0384-3

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