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Published in: Anatomical Science International 4/2015

01-09-2015 | Original Article

Axons from the medial habenular nucleus are topographically sorted in the fasciculus retroflexus

Authors: Hiroyuki Ichijo, Tomoko Toyama

Published in: Anatomical Science International | Issue 4/2015

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Abstract

We generated transgenic mice lines with a construct consisting of the zif268/egr1 promoter and the gene for the normal long-life yellow fluorescent protein (Venus) with a membrane localization sequence. One of the lines exhibited topographic labeling in the medial habenular nucleus (MHb) during postnatal development, which confirmed the previous findings that the medial, lateral, and dorsal areas of MHb project to the ventral, dorsal, and lateral parts of the interpeduncular nucleus, respectively. In addition, the membranous localization of the labeling allowed us to observe spacial arrangement of the labeled axons in the fasciculus retroflexus (FR) in the transgenic mice. Here, we report topographic sorting of the MHb axons in the FR. At postnatal day (P) 5 and P10, the labeled axons from the medial MHb were fasciculated and ran through the narrow path in the core of the FR. At P24, the labeled axons from the medial and dorsal MHb were fasciculated and ran through the broad path in the FR core. No labeling occurred in the lateral MHb throughout development; correspondingly, parts of the FR core remained unlabeled. The results indicated that the axons from the medial and dorsal areas of the MHb are grouped together in the FR of this transgenic line and are sorted out from the axons from the lateral MHb.
Literature
go back to reference Agetsuma M, Aizawa H, Aoki T, Nakayama R, Takahoko M, Goto M et al (2010) The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat Neurosci 13:1354–1356CrossRefPubMed Agetsuma M, Aizawa H, Aoki T, Nakayama R, Takahoko M, Goto M et al (2010) The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat Neurosci 13:1354–1356CrossRefPubMed
go back to reference Andres KH, von Duering M, Veh RW (1999) Subnuclear organization of the rat habenular complexes. J Comp Neurol 407:130–150CrossRefPubMed Andres KH, von Duering M, Veh RW (1999) Subnuclear organization of the rat habenular complexes. J Comp Neurol 407:130–150CrossRefPubMed
go back to reference Contestabile A, Villani L, Fasolo A, Franzoni MF, Gribaudo L, Oktedalen O et al (1987) Topography of cholinergic and substance P pathways in the habenulointerpeduncular system of the rat. An immunocytochemical and microchemical approach. Neuroscience 21:253–270PubMed Contestabile A, Villani L, Fasolo A, Franzoni MF, Gribaudo L, Oktedalen O et al (1987) Topography of cholinergic and substance P pathways in the habenulointerpeduncular system of the rat. An immunocytochemical and microchemical approach. Neuroscience 21:253–270PubMed
go back to reference Cuello AC, Emson PC, Paxinos G, Jessell T (1978) Substance P containing and cholinergic projections from the habenular. Brain Res 149:413–429CrossRefPubMed Cuello AC, Emson PC, Paxinos G, Jessell T (1978) Substance P containing and cholinergic projections from the habenular. Brain Res 149:413–429CrossRefPubMed
go back to reference Fahmy RG, Dass CR, Sun LQ, Chesterman CN, Khachigian LM (2003) Transcription factor Egr-1 supports FGF-dependent angiogenesis during neovascularization and tumor growth. Nat Med 9:1026–1032CrossRefPubMed Fahmy RG, Dass CR, Sun LQ, Chesterman CN, Khachigian LM (2003) Transcription factor Egr-1 supports FGF-dependent angiogenesis during neovascularization and tumor growth. Nat Med 9:1026–1032CrossRefPubMed
go back to reference Geisler S, Andres KH, Veh RW (2003) Morphologic and cytochemical criteria for the identification and delineation of individual subnuclei within the lateral habenular complex of the rat. J Comp Neurol 458:78–97CrossRefPubMed Geisler S, Andres KH, Veh RW (2003) Morphologic and cytochemical criteria for the identification and delineation of individual subnuclei within the lateral habenular complex of the rat. J Comp Neurol 458:78–97CrossRefPubMed
go back to reference Grady SR, Moretti M, Zoli M, Marks MJ, Zanardi A, Pucci L et al (2009) Rodent habenulointerpeduncular pathway expresses a large variety of uncommon nAChR subtypes, but only the alpha3beta4* and alpha3beta3beta4* subtypes mediate acetylcholine release. J Neurosci 29:2272–2282PubMedCentralCrossRefPubMed Grady SR, Moretti M, Zoli M, Marks MJ, Zanardi A, Pucci L et al (2009) Rodent habenulointerpeduncular pathway expresses a large variety of uncommon nAChR subtypes, but only the alpha3beta4* and alpha3beta3beta4* subtypes mediate acetylcholine release. J Neurosci 29:2272–2282PubMedCentralCrossRefPubMed
go back to reference Herkenham M, Nauta WJ (1977) Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol 173:123–146CrossRefPubMed Herkenham M, Nauta WJ (1977) Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol 173:123–146CrossRefPubMed
go back to reference Herkenham M, Nauta WJ (1979) Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187:19–47CrossRefPubMed Herkenham M, Nauta WJ (1979) Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187:19–47CrossRefPubMed
go back to reference Ichijo H (1999) Differentiation of the chick retinotectal topographic map by remodeling in specificity and refinement in accuracy. Dev Brain Res 117:199–211CrossRef Ichijo H (1999) Differentiation of the chick retinotectal topographic map by remodeling in specificity and refinement in accuracy. Dev Brain Res 117:199–211CrossRef
go back to reference Iwahori N, Nakamura K, Kameda S (1993) Terminal patterns of the fasciculus retroflexus in the interpeduncular nucleus of the mouse: a Golgi study. Anat Embryol 187:523–528CrossRefPubMed Iwahori N, Nakamura K, Kameda S (1993) Terminal patterns of the fasciculus retroflexus in the interpeduncular nucleus of the mouse: a Golgi study. Anat Embryol 187:523–528CrossRefPubMed
go back to reference Kim U, Chang SY (2005) Dendritic morphology, local circuitry, and intrinsic electrophysiology of neurons in the rat medial and lateral habenular nuclei of the epithalamus. J Comp Neurol 483:236–250CrossRefPubMed Kim U, Chang SY (2005) Dendritic morphology, local circuitry, and intrinsic electrophysiology of neurons in the rat medial and lateral habenular nuclei of the epithalamus. J Comp Neurol 483:236–250CrossRefPubMed
go back to reference Mroz ED, Brownstein MJ, Leeman SE (1976) Evidence for substance P in the habenulointerpeduncular tract. Brain Res 113:597–599CrossRefPubMed Mroz ED, Brownstein MJ, Leeman SE (1976) Evidence for substance P in the habenulointerpeduncular tract. Brain Res 113:597–599CrossRefPubMed
go back to reference Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87–90CrossRefPubMed Nagai T, Ibata K, Park ES, Kubota M, Mikoshiba K, Miyawaki A (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20:87–90CrossRefPubMed
go back to reference Okamoto H, Agetsuma M, Aizawa H (2012) Genetic dissection of the zebrafishhabenula, a possible switching board for selection of behavioral strategy to cope with fear and anxiety. Dev Neurobiol 72:386–394CrossRefPubMed Okamoto H, Agetsuma M, Aizawa H (2012) Genetic dissection of the zebrafishhabenula, a possible switching board for selection of behavioral strategy to cope with fear and anxiety. Dev Neurobiol 72:386–394CrossRefPubMed
go back to reference Sakamoto KM, Bardeleben C, Yates KE, Raines MA, Golde DW, Gasson JC (1991) 5′ upstream sequence and genomic structure of the human primary response gene, EGR-1/TIS8. Oncogene 6:867–871PubMed Sakamoto KM, Bardeleben C, Yates KE, Raines MA, Golde DW, Gasson JC (1991) 5′ upstream sequence and genomic structure of the human primary response gene, EGR-1/TIS8. Oncogene 6:867–871PubMed
go back to reference Shumake J, Edwards E, Gonzalez-Lima F (2003) Opposite metabolic changes in the habenula and ventral tegmental area of a genetic model of helpless behavior. Brain Res 963:274–281CrossRefPubMed Shumake J, Edwards E, Gonzalez-Lima F (2003) Opposite metabolic changes in the habenula and ventral tegmental area of a genetic model of helpless behavior. Brain Res 963:274–281CrossRefPubMed
go back to reference Stein I, Itin A, Einat P, Skaliter R, Grossman Z, Keshet E (1998) Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol Cell Biol 18:3112–3119PubMedCentralPubMed Stein I, Itin A, Einat P, Skaliter R, Grossman Z, Keshet E (1998) Translation of vascular endothelial growth factor mRNA by internal ribosome entry: implications for translation under hypoxia. Mol Cell Biol 18:3112–3119PubMedCentralPubMed
go back to reference Wirtshafter D, Asin KE, Pitzer MR (1994) Dopamine agonists and stress produce different patterns of Fos-like immunoreactivity in the lateral habenula. Brain Res 633:21–26CrossRefPubMed Wirtshafter D, Asin KE, Pitzer MR (1994) Dopamine agonists and stress produce different patterns of Fos-like immunoreactivity in the lateral habenula. Brain Res 633:21–26CrossRefPubMed
go back to reference Yamaguchi T, Danjo T, Pastan I, Hikida T, Nakanishi S (2013) Distinct roles of segregated transmission of the septo-habenular pathway in anxiety and fear. Neuron 78:537–544PubMedCentralCrossRefPubMed Yamaguchi T, Danjo T, Pastan I, Hikida T, Nakanishi S (2013) Distinct roles of segregated transmission of the septo-habenular pathway in anxiety and fear. Neuron 78:537–544PubMedCentralCrossRefPubMed
Metadata
Title
Axons from the medial habenular nucleus are topographically sorted in the fasciculus retroflexus
Authors
Hiroyuki Ichijo
Tomoko Toyama
Publication date
01-09-2015
Publisher
Springer Japan
Published in
Anatomical Science International / Issue 4/2015
Print ISSN: 1447-6959
Electronic ISSN: 1447-073X
DOI
https://doi.org/10.1007/s12565-014-0252-z

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